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系統識別號 U0026-1506201218065700
論文名稱(中文) 大腸桿菌細胞外膜蛋白 C 於 carbapenem 抗藥機制與致病毒性之角色
論文名稱(英文) The role of outer membrane protein C in Escherichia coli carbapenem-resistance and virulence
校院名稱 成功大學
系所名稱(中) 基礎醫學研究所
系所名稱(英) Institute of Basic Medical Sciences
學年度 100
學期 2
出版年 101
研究生(中文) 劉宜芳
研究生(英文) Yi-Fang Liu
學號 s58941379
學位類別 博士
語文別 英文
論文頁數 113頁
口試委員 指導教授-吳俊忠
口試委員-顏經洲
口試委員-鄧景浩
口試委員-柯文謙
口試委員-賴信志
口試委員-賈景山
中文關鍵字 大腸桿菌  抗藥性  細胞外膜蛋白  補體 
英文關鍵字 E. coli  carbapenem  OmpC  bactericidal activity  C1q  classical pathway 
學科別分類
中文摘要 大腸桿菌中的細胞外膜蛋白C作為細胞膜通透管道,可幫助細菌攝入養分和抗生素,也可將毒物排出菌體。超廣效抗生素carbapenems是目前臨床上最常使用來治療多重抗藥性的腸內菌,然而這些carbapenems 抗藥性的菌株的傳播可能成為治療上的一大問題。因此本研究主要的目的為探討carbapenem非敏感性大腸桿菌中的抗藥機轉與其毒力為何。首先,在1999年到2005年之間成大醫院菌株收集中,carbapenem非敏感性大腸桿菌比例由0% 增加至0.27%。共有這九株基因多元性的菌株同時對於第三代與第四代頭胞子黴素呈現抗藥性,並且都失去細胞外膜蛋白C的表現與合併CMY-2 AmpC乙內醯胺的產生。這些非敏感性菌株,若能表現野生細胞外膜蛋白C,則carbapenems與cefipime的敏感性可被回復。此外,由一株carbapenem敏感性菌株中建構其同源性細胞外膜蛋白C刪除突變株也發現對於carbapenems與cefipime的敏感性有明顯的下降,而互補菌株則又回復其敏感性。這些結果指出,細胞外膜蛋白C的失去對於carbapenem非敏感性大腸桿菌是非常重要的。接下來我們想證實是否細胞外膜蛋白C與大腸桿菌的致病毒力有關。在人類全血殺菌試驗中,細胞外膜蛋白C突變株在人類血液與血清中具有較高的生存能力,然而受到補體去活化的血清中則無殺菌效果。利用體外自然篩選模式所分離到的細胞外膜蛋白突變株也同時具有對carbapenems與殺菌活性的抵抗能力。此外,我們也證實細胞外膜蛋白C是一個主要的標的物供補體中C1q與抗體所形成的複合物結合,而細菌的生存能力也在重組細胞外膜蛋白C與抗C1q抗體的競爭下隨劑量的增加而逐漸回復,這些結果指出細胞外膜蛋白C之專一性抗體與補體中C1q分子的結合進而活化下游抗體依賴之典型補體路徑,來清除帶有細胞外膜蛋白C的大腸桿菌,由於人類血清中可偵測到抗細胞外膜蛋白C的抗體,故此蛋白可視為一免疫源。另一方面,部分由自然篩選實驗中取得的大腸桿菌會表現出因編碼區中氨基酸置換而產生的變化型細胞外膜蛋白C,這些菌株因此呈現ertapenem與meropenem有抗藥性,但卻對於imipenem與cefipime為敏感性的特殊抗藥性。總結,本研究顯示,大腸桿菌若失去細胞外膜蛋白C的表現不只可抵抗抗生素清除,除外也能逃脫由C1q與抗細胞外膜蛋白C抗體所活化的抗體依賴性典型補體殺菌活性。透過我們的研究也暗示著抗生素的使用需更加注意,才能避免細菌多種抗藥性與致病細菌的產生。
英文摘要 Outer membrane proteins C (OmpC) serve as the permeability channels in Escherichia coli to uptake the nutrients and antibiotics, and exclude toxins. A broad spectrum antibiotic, carbapenem, is often used to treat serious infections caused by multidrug-resistant Enterobacteriaceae isolates. The spread of carbapenem-resistant Enteribacteriaceae may lead to a serious therapeutic problem. The aims of this study were to investigate the resistant mechanisms and virulence in carbapenem-non-susceptible E. coli (CNS-EC). At first, we showed that the prevalence of CNS-EC increased from 0% to 0.27% between 1999 and 2005 at National Cheng Kung University Hospital. Totally 9 CNS-EC isolates with genetic diversity resisted to 3ed- and 4th- generation cephalosporins. All CNS-EC had a loss of OmpC expression combining with CMY-2 AmpC enzyme production. The susceptibilities of carbapenems and cefipime were restored by transformation of wild-type ompC into these isolates. Besides, an ompC deletion mutant constructed from a carbapenem susceptible isolate showed a significantly decreased carbapenems susceptibility, whereas the carbapenem susceptibility was restored in OmpC complementary strain. The result indicates the loss of OmpC expression is important in CNS-EC. We further investigated whether OmpC was also involved in the virulence. The human blood bactericidal assay showed that the ompC mutant had higher survival in blood and serum, but not in complement-inactivated serum. The OmpC mutant recovered from natural selection showed the resistance to both carbapenems and bactericidal activity. Besides, C1q interacted with E. coli through a complex of antibodies bound to OmpC as a major target. Bacterial survival was increased in the wild-type strain in a dose-dependent manner when free recombinant OmpC protein or anti-C1q antibody was added in human serum. These results demonstrated that the interaction of OmpC-specific antibody and C1q was the key step to initiate the antibody-dependent classical pathway for the clearance of OmpC-expressing E. coli. Anti-OmpC antibody was detected in human sera, indicating the OmpC is an immunogen. In addition, some naturally selective E. coli which expressed variant OmpC with the amino acid substitution in coding region revealed specially resistant patterns to ertapenem and meropenem, but not imipenem and cefipime. In conclusion, the loss of OmpC expression in E. coli not only resist to antibiotics but also escape from serum’s bactericidal effect mediated by the C1q and anti-OmpC antibody-dependent classical pathway. Our data imply that antibiotics usage should be cautious to prevent bacteria from multidrug resistant and virulence.
論文目次 中文摘要 i
Abstract ii
致謝 iii
Table of contents iv
List of tables ix
List of figures x
Abbreviations xi
Chapter 1. Introduction 1
1.1. Overview of carbapenems 1
1.1.1. General review of carbapenems resistant mechanisms in Enterobacteriaceae 1
1.1.1.1. β-lactamases 2
1.1.1.1.1. Plasmid-mediated AmpC β-lactamase 2
1.1.1.1.2. Carbapenemase 2
1.1.1.1.2.1. MBL 3
1.1.1.1.2.2. Non-MBL carbapenemases 3
1.1.1.2. Loss of outer membrane proteins (OMPs) 4
1.1.1.3. Over-expression of efflux pumps 4
1.2. The virulence of multidrug resistant bacteria 4
1.3. Overview of complement system 5
1.3.1. Classical pathway 5
1.3.2. Alternative pathway 6
1.3.3. Lectin pathway 7
1.3.4. MAC 7
1.3.5. Fragments from complement component in innate immunity, anaphylatoxins 7
1.4. Overview of Escherichia coli 8
1.4.1. Carbapenems resistance in E. coli 9
1.4.2. Complement activation and evasion by E. coli 10
1.4.2.1. Capsule 10
1.4.2.2. LPS 11
1.4.2.3. OmpA 11
1.4.2.4. Secreted proteins 12
1.5. OmpC of E. coli 12
1.6. Specific aims 14
Chapter 2. Materials and Methods 15
2.1. Bacterial strains 15
2.2. Primers & plasmids 15
2.3. Antimicrobial susceptibility 15
2.3.1. Susceptibility testing 15
2.3.1.1. Disk diffusion method.. 15
2.3.1.2. Minimum inhibitory concentration (MIC) 16
2.3.1.2.1. Agar dilution method 16
2.3.1.2.2. E-test 16
2.3.2. Detection of ESBL production 16
2.3.2.1. CLSI-recommended disk-diffusion confirmatory test 16
2.3.2.2. Double-disk synergy test 17
2.3.2.3. 2-MPA double-disk synergy test 17
2.3.3. β-Lactamase analysis 17
2.4. DNA manipulations 18
2.4.1. Genomic DNA extraction 18
2.4.2. Plasmid DNA extraction 18
2.4.3. Preparation of competent cells 19
2.4.3.1. Heat-shock transformation 19
2.4.3.2. Electroporation 19
2.4.4. Heat-shock transformation 20
2.4.5. Electroporation 20
2.4.6. Allelic exchange mutagenesis (for temperature sensitive plasmid) 20
2.4.7. Southern blot 21
2.4.7.1. DNA digestion, electrophoresis and DNA membrane preparation 21
2.4.7.2. Probe preparation 21
2.4.7.3. Hybridization and detection 22
2.4.8. Pulsed field gel electrophoresis (PFGE) 22
2.5. RNA manipulations 23
2.5.1. RNA extraction 23
2.5.2. Northern blot 23
2.6. Protein manipulations 24
2.6.1. OMPs extraction 24
2.6.2. Identification of OMPs 24
2.6.3. Protein concentration measurement 24
2.6.4. SDS-PAGE electrophoresis 24
2.6.5. Western blot 25
2.6.6. Recombinant OmpC protein (rOmpC) purification 25
2.6.7. Mouse polyclone antibody generation 26
2.6.8. Human anti-OmpC antibody purification..... 26
2.6.8.1. Protein coupling 26
2.6.8.2. Antibody purification 27
2.6.9. Protein structure prediction 27
2.7. Cell manipulations 27
2.7.1. Polymorphonuclear (PMN) cells isolation 27
2.7.2. Adhesion assay 28
2.7.3. Phagocytosis assay 28
2.8. Bacteria growth curve 28
2.9. Bactericidal assay 29
2.10. Natural selection of ompC mutated E. coli 29
2.11. Inhibition of the classical pathway by human IgG cleavage 29
2.12. Inhibition of the alternative pathway 30
2.13. Ligand overlap assay 30
2.14. Binding of C1q to E. coli... 31
2.15. Bactericidal assay with recombinant OmpC protein (rOmpC) and human C1q competition 31
2.16. Serological analysis of OmpC antibody 31
2.17. Statistical analysis 31
Chapter 3. Results 33
3.1. Characterization of carbapenem-non-susceptible E. coli isolates 33
3.1.1. Prevalence of carbapenem-non-susceptible E. coli isolates 33
3.1.2. Clinical characteristics 33
3.1.3. PFGE analysis 33
3.1.4. Susceptibility testing 34
3.1.5. β-Lactamase characterization 34
3.1.5.1. Confirmatory test, double-disk synergy test and 2-MPA double-disk synergy tests 35
3.1.5.2. bla PCR experiments, IEF and hydrolysis analysis 35
3.1.6. OMPs profiles 35
3.1.7. Sequence analysis of ompC 36
3.1.8. Expression of OmpC and OmpF in carbapenem-non-susceptible E. coli isolates 37
3.2. Role of OmpC in E. coli to both antibiotic susceptibility and human bactericidal activity 37
3.2.1. Construction of ompC mutant in carbapenem susceptible E. coli 2837-2/05 37
3.2.2. Effect of OmpC on antimicrobial susceptibility 38
3.2.3. Role of OmpC on human bactericidal activity 38
3.2.4. Role of OmpC on human bactericidal activity as strain independent manner 39
3.2.5. OmpC mediated blood bactericidal activity is not found in mice 39
3.3. Loss of OmpC in E. coli contributes to escape antibody-dependent bactericidal activity 40
3.3.1. OmpC mediated antibody-dependent classical pathway 40
3.3.2. OmpC is not major in bactericidal activity mediated by alternative pathway 40
3.3.3. C1q binds to E. coli OmpC in an antibody-dependent manner 40
3.3.4. OmpC is not major in C1q mediated antibody-independent classical pathway 41
3.3.5. Role of the human anti-OmpC specific antibody mediated classical pathway on bactericidal activity 41
3.3.6. OmpC is a major immunogen 42
3.4. Role of OmpC in interacting with human PMNs 42
3.4.1. Adhesion and phagocytosis ability of human PMNs 42
3.5. OmpC expression in E. coli clinical isolates 43
3.6. Natural selection for ompC mutants 43
3.6.1. Natural selection of E. coli from carbapenem containing medium 43
3.6.2. Natural selection of mutants resist to bactericidal activity 44
3.6.3. Characterization of variant OmpC in natural selective E. coli 44
3.6.3.1. The role of variant OmpC in antimicrobial susceptibility 45
3.6.3.2. The identification of variant OmpC 45
Chapter 4. Discussion 46
4.1. The increasing rate of carbapenem resistant in E. coli 46
4.2. The resistant mechanisms of carbapenem in E. coli 46
4.3. Role of OmpC in E. coli to serum bactericidal activity 48
4.4. Bactericidal activity through the anti-OmpC specific antibody- dependent classical pathway 49
4.5. Bactericidal activity through the antibody-independent classical pathway and other pathway 50
4.6. OmpC as the vaccine candidate 51
4.7. The role of variant OmpC in antibiotic susceptibility 52
4.8. Loss of OmpC contributes to both antibiotic resistance and escaping antibody-dependent bactericidal activity 53
4.9. Conclusions 54
Chapter 5. References 55
Chapter 6. Tables 73
Chapter 7. Figures 82
Chapter 8. Appendix 104
8.1. The structures of carbapenems 104
8.2. Classification of carbapenemases 105
8.3. The schematic description of complement system 106
8.4. BLOSUM62 Substitution Matrix 107
8.5. Chemical and reagents 108
8.6. Media and solutions 110
自述與發表文章 114
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