Chapter 29 : The Tao of Urease

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

The Tao of Urease, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap29-1.gif /docserver/preview/fulltext/10.1128/9781555818340/9781555810825_Chap29-2.gif


This chapter describes the role of bacterial urease in infection, the structure of urease, and the genetic organization and regulation of urease genes. When urease is produced by uropathogens in an infected urinary tract, the hydrolysis of urea increases the ammonia concentration in the urine, and there is a subsequent elevation of the urine pH. The exact mechanism responsible for the increased level of survival of the pathogen and the damage associated with urease can only be inferred. Increased bacterial colonization of the urinary tract might result from the generation of an easily assimilated nitrogen source and/or from alkalinization of the urine to a more favorable pH for growth. Urease is produced in abundance by , a gram-negative curved or spiral bacterium that lives in the mucous layer overlaying the gastric epithelium. -infected gastric mucosa is characterized by a predominant neutrophil accumulation, and ammonia is thought to enhance a neutrophil-dependent cytocidal activity. The species urease gene cluster appears to code for more accessory polypeptides than are found in and species urease gene clusters. Expression of the plasmid-encoded urease genes appears to be regulated by a transcriptional activator termed UreR. Analysis of the chromosomal locus indicates that it contains only seven of the urease genes, , , , , , , and . Therefore, in contrast to the inducible gene clusters, no additional gene products are required for the constitutive expression of urease in .

Citation: Collins C. 1994. The Tao of Urease, p 437-449. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch29
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Role of urease in the formation of struvite stones. Adapted from Griffith and Osborne ( ). Reprinted with permission of S. Karger AG, Basel.

Citation: Collins C. 1994. The Tao of Urease, p 437-449. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch29
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Maps of various bacterial urease gene clusters. Shown are the relative sizes and orientations of the chromosomal urease genes ( ), and urease genes ( ), the plasmid-encoded and urease genes ( ), urease genes ( ), and sp. strain TB-90 urease genes ( ). Open boxes indicate the positions of each gene (). The oval represents Nac, the nitrogen assimilation control protein ( ). The arrow points to the Nac-binding site, located approximately 90 nucleotides upstream of in ( ).

Citation: Collins C. 1994. The Tao of Urease, p 437-449. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch29
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Similarity between the amino acid sequences of UreA (structural subunit) and UreD (accessory polypeptide) from various bacterial species. A dendrogram representation of the clustering relationships between the amino acid sequences is shown. The horizontal branch lengths are proportional to the similarities between the sequences. A pairwise alignment of the sequences was performed by the algorithm of Needleman and Wunsch ( ) by using a re-scaled version of the scoring matrix of Dayhoff et al. ( ), as found in the Genetics Computer Group Sequence Analysis Software package, version 7.0.2 ( ). The similarity scores obtained were used to create a clustering order by the unweighted pair-group method by using arithmetic averages ( ). For the first 101 amino acids of UreA were analyzed UreH is thought to be equivalent to UreD of the other clusters.

Citation: Collins C. 1994. The Tao of Urease, p 437-449. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch29
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Beeson, P. B.,, and D. Rowley. 1959. The anticomplementary effect of kidney tissue. Its association with ammonia production. J. Exp. Med. 110: 695 698.
2. Bender, R. A. 1991. The role of the NAC protein in the nitrogen regulation of Klebsiella aerogenes. Mol. Microbiol. 5: 2575 2580.
3. Bender, R. A.,, P. M. Snyder,, R. Bueno,, M. Quinto,, and B. Magasanik. 1983. Nitrogen regulation system of Klebsiella aerogenes: the nac gene. J. Bacteriol. 156: 444 446.
4. Blaser, M. J. 1992. Helicobacter pylori: its role in disease. Clin. Infect. Dis. 15: 386 393.
5. Braude, A. I.,, and J. Siemienski. 1960. Role of bacterial urease in experimental pyelonephritis. J. Bacteriol. 80: 171 179.
6. Breitenbach, J. M.,, and R. P. Hausinger. 1988. Proteus mirabilis urease: partial purification and inhibition by boric acid and boronic acids. Biochem. J. 250: 917 920.
7. Collins, C. M. Unpublished data.
8. Collins, C. M.,, and S. Falkow. 1990. Genetic analysis of Escherichia coli urease genes: evidence for two distinct loci. J. Bacteriol. 172: 7138 7144.
9. Collins, C. M.,, and D. Gutman. Unpublished data.
10. Collins, C. M.,, and D. M. Gutman. 1992. Insertional inactivation of an Escherichia coli urease gene by 1S3411. J. Bacteriol. 174: 883 888.
11. Collins, C. M.,, D. M. Gutman,, and H. Laman. 1993. Identification of a nitrogen-regulated promoter controlling expression of Klebsiella pneumoniae urease genes. Mol. Microbiol. 8: 187 198.
12. Cussac, V.,, R. L. Ferrero,, and A. Labigne. 1992. Expression of Helicobacter pylori urease genes in Escherichia coli grown under nitrogen-limiting conditions. J. Bacteriol. 174: 2466 2473.
13. Dayhoff,' M. O.,, R. M. Schwartz,, and B. C. Orcutt,. 1978. Matrices for detecting distant relationships, p. 353 358. In M. O. Dayhoff (ed.), The Atlas of Protein Sequence and Structure. National Biomedical Research Foundation, Washington, D.C..
14. Delisle, G. J. 1977. Multiple forms of urease in cytoplasmic fractions of Ureaplasma urealyticum. J. Bacteriol. 130: 1390 1392.
15. Devereux, J.,, P. Haeberli,, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387 395.
16. DeVivo, M. J.,, P. R. Fine,, G. R. Cutter,, and H. M. Maetz. 1984. The risk of renal calculi in spinal cord injury patients. J. Urol. 131: 857 860.
17. Dixon, N. E.,, R. L. Blakeley,, and B. Zerner. 1980. Jack bean urease (EC III. The involvement of active-site nickel ion in inhibition by β-mercaptoethanol, phosphoramidate, and fluoride. Can. J. Biochem. 58: 481 488.
18. D'Orazio, S. E. F.,, and C. M. Collins. Unpublished data.
19. D'Orazio, S. E. F.,, and C. M. Collins. 1993. Characterization of a plasmid-encoded urease gene cluster found among members of the family Enterobacteriaceae. J. Bacteriol. 175: 1860 1864.
20. D'Orazio, S. E. F.,, and C. M. Collins. 1993. The plasmid-encoded urease gene cluster of the Enterobacteriaceae is positively regulated by UreR, a member of the AraC family of transcriptional activators. J. Bacteriol. 175: 3459 3467.
21. Dunn, B. E.,, G. P. Campbell,, G. I. Perez-Perez,, and M. J. Blaser. 1990. Purification and characterization of urease from Helicobacter pylori. J. Biol. Chem. 265: 9464 9469.
22. Eaton, K.,, C. L. Brooks,, D. R. Morgan,, and S. Krakowka. 1991. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect. Immun. 59: 2470 2475.
23. Fowler, J. E. J. 1984. Bacteriology of branched renal calculi and accompanying urinary tract infection. J. Urol. 131: 213 215.
24. Friedrich, B.,, and B. Magasanik. 1977. Urease of Klebsiella aerogenes: control of its synthesis by glutamine synthetase. J. Bacteriol. 131: 446 452.
25. Gallegos, M.-T.,, C. Michan,, and J. L. Ramos. 1993. The XylS/AraC family of regulators. Nucleic Acids Res. 21: 807 810.
26. Gatermann, S.,, J. John,, and R. Marre. 1988. Staphylococcus saprophyticus urease: characterization and contribution to uropathogenicity in unobstructed urinary tract infection of rats. Infect. Immun. 57: 110 116.
27. Gatermann, S.,, and R. Marre. 1989. Cloning and expression of Staphylococcus saprophyticus urease gene sequences in Staphylococcus carnosus and contribution of the enzyme to virulence. Infect. Immun. 57: 2998 3002.
28. Goss, T. G.,, and R. A. Bender. Personal communication.
29. Grant, R. B.,, J. L. Penner,, J. N. Hennesey,, and B. J. Jackowski. 1981. Transferable urease activity in Providencia stuartii. J. Clin. Microbiol. 13: 561 565.
30. Grenbro, L.,, H. Hedelin,, and S. Petterson. 1988. Urinary infection stones caused by Ureaplasma urealyticum: a review. Scand. J. Infect. Dis. 53: 46 49.
31. Griffith, D. P.,, F. Khonsari,, J. H. Skurnick,, K. E. James,, and V. A. C. S. Group. 1988. A randomized trial of acetohydroxamic acid for the treatment and prevention of infection-induced urinary stones in spinal cord injury patients. J. Urol. 140: 318 324.
32. Griffith, D. P.,, D. M. Musher,, and C. Bin. 1976. Urease: the primary cause of infection-induced urinary stones. Invest. Urol. 13: 346 350.
33. Griffith, D. P.,, and C. A. Osborne. 1987. Infection (urease) stones. Min. Electrol. Metab. 13: 278.
34. Hausinger, R. P. 1987. Nickel utilization by microorganisms. Microbiol. Rev. 51: 22 24.
35. Hawtin, P. R.,, A. R. Stacey,, and D. G. Newell. 1990. Investigation of the structure and location of the urease of Helicobacter pylori using monoclonal antibodies. J. Gen. Microbiol. 136: 1995 2000.
36. Hazell, S. L.,, and A. Lee. 1986. Campylobacter pyloridis, urease, hydrogen ion back diffusion, and gastric ulcers. Lancet ii: 15 17.
37. Hu, L.,, and H. L. T. Mobley. 1990. Purification and N-terminal analysis of urease from Helicobacter pylori. Infect. Immun. 58: 992 998.
38. Hu, L.-T.,, P. A. Foxall,, R. Russell,, and H. L. T. Mobley. 1992. Purification of recombinant Helicobacter pylori urease apoenzyme encoded by ureA and ureB. Infect. Immun. 60: 2657 2666.
39. Janssen, D. B.,, W. J. A. Habets,, J. T. Mamgg,, and C. van der Drift. 1982. Nitrogen control in Pseudomonas aeruginosa: mutants affected in the synthesis of glutamine synthetase, urease, and NADP-dependent glutamate dehydrogenase. J. Bacteriol. 151: 22 28.
40. Johnson, D. E.,, R. G. Russell,, C. V. Lockatell,, J. C. Zulty,, J. W. Warren,, and H. L. T. Mobley. 1993. Contribution of Proteus mirabilis urease to persistence, urolithiasis, and acute pyelonephritis in a mouse model of ascending urinary tract infection. Infect. Immun. 61: 2748 2754.
41. Jones, B. D.,, C. V. Lockatell,, D. E. Johnson,, J. W. Warren,, and H. L. T. Mobley. 1990. Construction of a urease-negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect. Immun. 58: 1120 1123.
42. Jones, B. D.,, and H. L. T. Mobley. 1988. Proteus mirabilis urease: genetic organization, regulation, and expression of structural genes. J. Bacteriol. 170: 3342 3349.
43. Jones, B. D.,, and H. L. T. Mobley. 1989. Proteus mirabilis urease: nucleotide sequence determination and comparison with jack bean urease. J. Bacteriol. 171: 6414 6422.
44. Kenny, G. E.,, and F. D. Cartwright. 1977. Effect of urea concentration on growth of Ureaplasma urealyticum (T-strain mycoplasma). J. Bacteriol. 132: 144 150.
45. Labigne, A.,, V. Cussac,, and P. Courcoux. 1991. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J. Bacteriol. 173: 1920 1931.
46. Lee, M. H.,, S. B. Mulrooney,, and R. P. Hausinger. 1990. Purification, characterization, and in vivo recombination of Klebsiella aerogenes urease apoenzyme. J. Bacteriol. 172: 4427 4431.
47. Lee, M. H.,, S. B. Mulrooney,, M. J. Renner,, Y. Markowicz,, and R. P. Hausinger. 1992. Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureD, ureE, ureF, ureG) are involved in nickel metallocenter biosynthesis. J. Bacteriol. 174: 4324 4330.
48. Lee, M. H.,, H. S. Prankratz,, S. Wang,, R. A. Scott,, M. G. Finnegan,, M. K. Johnson,, J. A. Ippolito,, D. W. Christianson,, and R. P. Hausinger. 1993. Purification and characterization of Klebsiella aerogenes UreE protein: a nickel binding protein that functions in urease metallo center assembly. Prot. Sci. 2: 1042 1052.
49. Lerner, S. P.,, M. J. Gleeson,, and D. P. Griffith. 1989. Infection stones. J. Urol. 141: 753 758.
50. Macaluso, A.,, E. A. Best,, and R. A. Bender. 1990. Role of the nac gene product in the nitrogen regulation of some NTR-regulated operons of Klebsiella aerogenes. J. Bacteriol. 172: 7249 7255.
51. MacLaren, D. M.,, and P. G. H. Peerbooms,. 1986. Urinary infections by urea splitting microorganisms. In A. W. Brumfit (ed.), Microbial Diseases in Nephrology. John Wiley & Sons, New York.
52. Maeda, M.,, M. Hidaka,, A. Nakamura,, H. Masaki,, and T. Uozumi. 1994. Cloning, sequencing, and expression of the thermophilic Bacillus sp. strain TB-90 urease gene complex in Escherichia coli. J. Bacteriol. 176: 432 442.
53. Magasanik, B.,, and F. C. Neidhardt,. 1987. Regulation of carbon and nitrogen utilization, p. 1318 1325. In F. C. Neidhardt,, J. L. Ingraham,, K. B. Low,, B. Magasanik,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington D.C..
54. Mai, U. E. H.,, G. I. Perez-Perez,, J. B. Allen,, S. M. Wahl,, M. J. Blaser,, and P. D. Smith. 1992. Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J. Exp. Med. 175: 517 525.
55. Maier, T.,, A. Jacob),, M. Sauter,, and A. Hock. 1993. The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J. Bacteriol. 175: 630 635.
56. Marshall, B. J.,, L. Barret,, C. Prakesh,, R. McCallum,, and R. Guerrant,. 1988. Protection of Campylobacter pyloridis but not Campylobacter jejuni against acid susceptibility by urea, p. 402 403. In B. Kaijserand, E. Falsen (ed.), Campylobacter IV. University of Goteborg, Goteborg, Sweden.
57. McLean, R. J. C.,, J. C. Nickel,, K.-J. Cheng,, and J. W. Costerton. 1988. The ecology and pathogenicity of urease-producing bacteria in the urinary tract. Crit. Rev. Microbiol. 16: 37 79.
58. Mertz, A.,, S. Batsford,, E. Curschellas,, M. Kist,, and K. Gondolf. 1991. Cationic Yersinia antigen-induced chronic allergic arthritis in rats. J. Clin. Invest. 88: 632 642.
59. Milkier, O. E. J.,, J. A. Andersen,, M. E. Appier,, C. E. Benjamin,, J. G. Edwards,, D. T. Humphrey,, and E. M. Shearer. 1982. Flurofamide: a potential inhibitor of bacterial urease with a potential clinical utility in the treatment of infection induced urinary stones. J. Urol. 127: 346 350.
60. Mobley, H. L. T.,, G. R. Chippendale,, M. H. Fraiman,, J. H. Tenney,, and J. W. Warren. 1985. Variable phenotypes of Providencia stuartii due to plasmid-encoded traits. J. Clin. Microbiol. 22: 851 853.
61. Mobley, H. L. T.,, G. R. Chippendale,, K. G. Swihart,, and R. A. Welch. 1991. Cytotoxicity of the HmpA hemolysis and urease of Proteus mirabilis and Proteus vulgaris against cultured human renal proximal tubular epithelial cells. Infect. Immun. 59: 2036 2042.
62. Mobley, H. L. T.,, and R. P. Hausinger. 1989. Microbial ureases: significance, regulation, and molecular characterization. Microbiol. Rev. 53: 85 108.
63. Mobley, H. L. T.,, B. D. Jones,, and A. E. Jerse. 1986. Cloning of urease gene sequences from Providencia stuartii. Infect. Immun. 54: 161 169.
64. Mobley, H. L. T.,, and J. W. Warren. 1987. Urease-positive bacteriuria and obstruction of long-term urinary catheters. J. Clin. Microbiol. 25: 2216 2217.
65. Mulrooney, S. B.,, and R. P. Hausinger. 1990. Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation. J. Bacteriol. 172: 5837 5843.
66. Mulrooney, S. B.,, M. J. Lynch,, H. L. T. Mobley,, and R. P. Hausinger. 1988. Purification, characterization, and genetic organization of recombinant Providencia stuartii urease expressed by Escherichia coli. J. Bacteriol. 170: 2202 2207.
67. Musher, D. M.,, D. P. Griffith,, D. Yawn,, and R. D. Rossen. 1975. Role of urease in pyelonephritis resulting from urinary tract infection with Proteus. J. Infect. Dis. 131: 177 181.
68. Needleman, S. B.,, and C. D. Wunsch. 1970. A general method applicable to the search for similarity in the amino acid sequence of two proteins. J. Mol. Biol. 48: 443 453.
69. Nicholson, E. B.,, E. A. Concaugh,, P. A. Foxall,, M. D. Island,, and H. L. T. Mobley. 1993. Proteus mirabilis urease: transcriptional regulation by UreR. J. Bacteriol. 175: 465 473.
70. Nicholson, E. B.,, E. A. Concaugh,, and H. L. T. Mobley. 1991. Proteus mirabilis urease: use of a ureA-lacZ fusion demonstrates that induction is highly specific for urea. J. Bacteriol. 59: 3360 3365.
71. Nomura, A.,, G. N. Stemmermann,, P.-H. Chyou,, I. Kato,, G. I. Perez-Perez,, and M. J. Blaser. 1991. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N. Engl. J. Med. 325: 1132 1136.
72. Parsonnet, J.,, G. D. Friedman,, D. P. Vandersteen,, Y. Chang,, J. H. Vogelman,, N. Orentreich,, and R. K. Sibley. 1991. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 325: 1121 1131.
73. Pickering, W. J.,, and D. F. Birch. 1989. Bacteriologic and serologic findings in experimental pyelonephritis caused by Ureaplasma urealyticum. Infect. Immun. 57: 1235 1239.
74. Probst, P.,, E. Hermann,, K.-H. Meyer zum Buschenfelde,, and B. Fleischer. 1993. Identification of the Yersinia enterocolitica urease B subunit as a target antigen for human synovial T lymphocytes in reactive arthritis. Infect. Immun. 61: 4507 4509.
75. Przybyla, A. E.,, J. Robbins,, N. Menon,, and H. D. J. Peck. 1992. Structure/function relationships among the nickel-containing hydrogenases. FEMS Microbiol. Rev. 88: 109 136.
76. Romano, N.,, R. La Litica,, and D. R. Alesi. 1986. Energy production in Ureaplasma urealyticum. Pediatr. Infect. Dis. J. 5: S308 S312.
77. Rosenstein, I.,, J. M. T. Hamilton-Miller,, and W. Brumfit. 1980. The effect of acetohydroxamic acids on the induction of bacterial ureases. Invest. Urol. 18: 112 114.
78. Schwada, A.,, and R. A. Bender. 1993. The nac (nitrogen assimilation control) gene from Klebsiella aerogenes. J. Bacteriol. 175: 2107 2115.
79. Segal, E. D.,, J. Shon,, and L. S. Tompkins. 1992. Characterization of Helicobacter pylori urease mutants. Infect. Immun. 60: 1883 1889.
80. Senior, B. W. 1983. Proteus morganii is less frequently associated with urinary tract infections than Proteus mirabilis—an explanation. J. Med. Microbiol. 16: 317 322.
81. Sheath, P. H. A.,, and R. R. Sokal. 1973. Numerical Taxonomy. W. H. Freeman & Co., San Francisco.
82. Sizer, I. W. 1941. Temperature activation of the urease-urea system using urease of Proteus vulgaris. J. Bacteriol. 41: 511 527.
83. Skurnik, M.,, S. Batsford,, A. Mertz,, E. Schiltz,, and P. Toivanen. 1993. The putative arthritogenic cationic 19-kilodalton antigen of Yersinia enterocolitica is a urease β subunit. Infect. Immun. 61: 2498 2504.
84. Smoot, D. T.,, H. L. T. Mobley,, G. R. Chippendale,, J. F. Lewison,, and J. H. Resau. 1990. Helicobacter pylori urease activity is toxic to human gastric epithelial cells. Infect. Immun. 58: 1992 1994.
85. Stetnke, G. W.,, J. A. Robertson,, and M. Nhan. 1987. Purification of urease from Ureaplasma urealyticum. Can. J. Microbiol. 33: 857 862.
86. Suzuki, M.,, S. Miura,, M. Suematsu,, D. Fukumura,, I. Kurose,, H. Suzuki,, A. Kai,, Y. Kudoh,, M. Ohashi,, and M. Tsuchiya. 1992. Helicobacter pylori-associated ammonia production enhances neutrophil-dependent gastric mucosal cell injury. Am. J. Physiol. 263: G719 G725.
87. Takebe, S.,, A. Numata,, and K. Kobashi. 1984. Stone formation by Ureaplasma urealyticum in human urine and its prevention by urease inhibitors. J. Clin. Microbiol. 20: 869 873.
88. Takeuchi, H.,, K. Kobashi,, and O. Yoshida. 1980. Prevention of infected urinary stones in rats by urease inhibitor. Invest. Urol. 18: 102 105.
89. Thirkell, D.,, A. D. Myles,, B. L. Precious,, J. S. Frost,, J. C. Woodall,, M. G. Burdon,, and W. C. Russell. 1989. The urease of Ureaplasma urealyticum. J. Gen. Microbiol. 135: 315 323.
90. Todd, M. J.,, and R. P. Hausinger. 1987. Purification and characterization of the nickel-containing multicomponent urease fron Klebsiella aerogenes. J. Biol. Chem. 262: 5963 5967.
91. Totten, P. A.,, J. C. Lara,, and S. Lory. 1990. The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J. Bacteriol. 172: 389 396.


Generic image for table
Table 1

Urease gene transcriptional activators

Citation: Collins C. 1994. The Tao of Urease, p 437-449. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch29

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error