细菌附属敏感性：优化药物治疗的新思路

doi:10.11843/j.issn.0366-6964.2022.10.005

Abstract

Abstract: “Cross resistance” (CR) is a phenomenon in which the bacteria have evolved to resist different types of antimicrobial molecules with similar structure or mechanisms of action, while "collateral sensitivity" (CS) can be defined as a situation where the bacteria have developed resistance to one antibiotic showed increased susceptibility to another antibiotic. The evolution of bacterial resistance is a complicated process that can either lead to cross resistance or collateral sensitivity under the selection pressure from antibiotics. Recently, CS has been proposed as a promising alternative approach to counteract the rising problem of antibiotic resistance. To better understand the mechanisms by which bacterial collateral sensitivity has been evolved and the application prospect of CS, in this review, we summarized our current knowledges on key factors influencing the bacterial collateral sensitivity and the regularities of CS. We also discuss directions and challenges for developing CS-informed treatment strategies.

Key words: bacteria resistance, collateral sensitivity, drug revolution resistance

CLC Number:

S859.7

HUANG Yingran,YE Xinqing,LIU Juan,YU Yang. Bacterial Collateral Sensitivity:A New Perspective to Optimize Treatments[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(10): 3316-3325.

References 63

[1]	ESTERLY J S, WAGNER J, MCLAUGHLIN M M, et al. Evaluation of clinical outcomes in patients with bloodstream infections due to gram-negative bacteria according to carbapenem MIC stratification[J]. Antimicrob Agents Chemother, 2012, 56(9):4885-4890.
[2]	LAXMINARAYAN R. Antibiotic effectiveness:balancing conservation against innovation[J]. Science, 2014, 345(6202):1299-1301.
[3]	IMAMOVIC L, SOMMER M O A. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development[J]. Sci Transl Med, 2013, 5(204):204ra132.
[4]	LÁZÁR V, SINGH G P, SPOHN R, et al. Bacterial evolution of antibiotic hypersensitivity[J]. Mol Syst Biol, 2013, 9(1):700.
[5]	PÁL C, PAPP B, LÁZÁR V. Collateral sensitivity of antibiotic-resistant microbes[J]. Trends Microbiol, 2015, 23(7):401-407.
[6]	BAYM M, STONE L K, KISHONY R. Multidrug evolutionary strategies to reverse antibiotic resistance[J]. Science, 2016, 351(6268):eaad3292.
[7]	ZHAO B Y, SEDLAK J C, SRINIVAS R, et al. Exploiting temporal collateral sensitivity in tumor clonal evolution[J]. Cell, 2016, 165(1):234-246.
[8]	IMAMOVIC L, ELLABAAN M M H, MACHADO A M D, et al. Drug-driven phenotypic convergence supports rational treatment strategies of chronic infections[J]. Cell, 2018, 172(1-2):121-134.
[9]	DHAWAN A, NICHOL D, KINOSE F, et al. Collateral sensitivity networks reveal evolutionary instability and novel treatment strategies in ALK mutated non-small cell lung cancer[J]. Sci Rep, 2017, 7(1):1232.
[10]	JENSEN P B, HOLM B, SORENSEN M, et al. In vitro cross-resistance and collateral sensitivity in seven resistant small-cell lung cancer cell lines:preclinical identification of suitable drug partners to taxotere, taxol, topotecan and gemcitabin[J]. Br J Cancer, 1997, 75(6):869-877.
[11]	PLUCHINO K M, HALL M D, GOLDSBOROUGH A S, et al. Collateral sensitivity as a strategy against cancer multidrug resistance[J]. Drug Resist Updat, 2012, 15(1-2):98-105.
[12]	WANG L Q, DE OLIVEIRA R L, HUIJBERTS S, et al. An acquired vulnerability of drug-resistant melanoma with therapeutic potential[J]. Cell, 2018, 173(6):1413-1425.
[13]	KIM S, LIEBERMAN T D, KISHONY R. Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance[J]. Proc Natl Acad Sci U S A, 2014, 111(40):14494-14499.
[14]	NICHOL D, RUTTER J, BRYANT C, et al. Antibiotic collateral sensitivity is contingent on the repeatability of evolution[J]. Nat Commun, 2019, 10(1):334.
[15]	HERENCIAS C, RODRÍGUEZ-BELTRÁN J, LEÓN-SAMPEDRO R, et al. Collateral sensitivity associated with antibiotic resistance plasmids[J]. eLife, 2021, 10:e65130
[16]	ROSENKILDE C E H, MUNCK C, PORSE A, et al. Collateral sensitivity constrains resistance evolution of the CTX-M-15 β-lactamase[J]. Nat Commun, 2019, 10(1):618.
[17]	ROEMHILD R, ANDERSSON D I. Mechanisms and therapeutic potential of collateral sensitivity to antibiotics[J]. PLoS Pathog, 2021, 17(1):e1009172.
[18]	KNOPP M, ANDERSSON D I. Predictable phenotypes of antibiotic resistance mutations[J]. mBio, 2018, 9(3):e00770-18.
[19]	ANDERSSON D I, HUGHES D. Antibiotic resistance and its cost:is it possible to reverse resistance?[J]. Nat Rev Microbiol, 2010, 8(4):260-271.
[20]	VOGWILL T, KOJADINOVIC M, MACLEAN R C. Epistasis between antibiotic resistance mutations and genetic background shape the fitness effect of resistance across species of Pseudomonas[J]. Proc Biol Sci, 2016, 283(1830):20160151.
[21]	BENNETT A F, LENSKI R E. An experimental test of evolutionary trade-offs during temperature adaptation[J]. Proc Natl Acad Sci U S A, 2007, 104(S1):8649-8654.
[22]	VELICER G J, SCHMIDT T M, LENSKI R E. Application of traditional and phylogenetically based comparative methods to test for a trade-off in bacterial growth rate at low versus high substrate concentration[J]. Microb Ecol, 1999, 38(3):191-200.
[23]	PALMER A C, KISHONY R. Opposing effects of target overexpression reveal drug mechanisms[J]. Nat Commun, 2014, 5(1):4296.
[24]	TOPRAK E, VERES A, MICHEL J B, et al. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection[J]. Nat Genet, 2012, 44(1):101-105.
[25]	LÁZÁR V, NAGY I, SPOHN R, et al. Genome-wide analysis captures the determinants of the antibiotic cross-resistance interaction network[J]. Nat Commun, 2014, 5(1):4352.
[26]	DRAGOSITS M, MOZHAYSKIY V, QUINONES-SOTO S, et al. Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli[J]. Mol Syst Biol, 2013, 9:643.
[27]	OSHIMA T, AIBA H, MASUDA Y, et al. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12[J]. Mol Microbiol, 2002, 46(1):281-291.
[28]	VENKATESH B, BABUJEE L, LIU H, et al. The Erwinia chrysanthemi 3937 PhoQ sensor kinase regulates several virulence determinants[J]. J Bacteriol, 2006, 188(8):3088-3098.
[29]	ROEMHILD R, LINKEVICIUS M, ANDERSSON D I. Molecular mechanisms of collateral sensitivity to the antibiotic nitrofurantoin[J]. PLoS Biol, 2020, 18(1):e3000612.
[30]	BRYANT D W, MCCALLA D R. Nitrofuran induced mutagenesis and error prone repair in Escherichia coli[J]. Chem-Biol Interact, 1980, 31(2):151-166.
[31]	HUISMAN O, D'ARI R. An inducible DNA replication-cell division coupling mechanism in E. coli[J]. Nature, 1981, 290(5809):797-799.
[32]	BI E, LUTKENHAUS J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring[J]. J Bacteriol, 1993, 175(4):1118-1125.
[33]	MIZUSAWA S, GOTTESMAN S. Protein degradation in Escherichia coli:The lon gene controls the stability of sulA protein[J]. Proc Natl Acad Sci U S A, 1983, 80(2):358-362.
[34]	AULIN L B S, LIAKOPOULOS A, VAN DER GRAAF P H, et al. Design principles of collateral sensitivity-based dosing strategies[J]. Nat Commun, 2021, 12(1):5691.
[35]	ARDELL S M, KRYAZHIMSKIY S. The population genetics of collateral resistance and sensitivity[J]. eLife, 2021, 10:e73250.
[36]	APJOK G, BOROSS G, NYERGES Á, et al. Limited evolutionary conservation of the phenotypic effects of antibiotic resistance mutations[J]. Mol Biol Evol, 2019, 36(8):1601-1611.
[37]	CHEN H L, JIANG Y, LI M M, et al. Acquisition of tigecycline resistance by carbapenem-resistant Klebsiella pneumoniae confers collateral hypersensitivity to aminoglycosides[J]. Front Microbiol, 2021, 12:674502.
[38]	GAGNEUX S, LONG C D, SMALL P M, et al. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis[J]. Science, 2006, 312(5782):1944-1946.
[39]	RODRíGUEZ-ROJAS A, MACIÁ M D, COUCE A, et al. Assessing the emergence of resistance:the absence of biological cost in vivo may compromise fosfomycin treatments for P. Aeruginosa infections[J]. PLoS One, 2010, 5(4):e10193.
[40]	BJOÖRKMAN J, NAGAEV I, BERG O G, et al. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance[J]. Science, 2000, 287(5457):1479-1482.
[41]	MAISNIER-PATIN S, PAULANDER W, PENNHAG A, et al. Compensatory evolution reveals functional interactions between ribosomal proteins S12, L14 and L19[J]. J Mol Biol, 2007, 366(1):207-215.
[42]	BARBOSA C, TREBOSC V, KEMMER C, et al. Alternative evolutionary paths to bacterial antibiotic resistance cause distinct collateral effects[J]. Mol Biol Evol, 2017, 34(9):2229-2244.
[43]	JONES D F. Proceedings of the sixth International congress of genetics[M]. New York:Brooklyn Botanic Garden, 1932.
[44]	MIRA P M, CRONA K, GREENE D, et al. Rational design of antibiotic treatment plans:a treatment strategy for managing evolution and reversing resistance[J]. PLoS One, 2015, 10(9):e0139387.
[45]	MALTAS J, WOOD K B. Pervasive and diverse collateral sensitivity profiles inform optimal strategies to limit antibiotic resistance[J]. PLoS Biol, 2019, 17(10):e3000515.
[46]	OZ T, GUVENEK A, YILDIZ S, et al. Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution[J]. Mol Biol Evol, 2014, 31(9):2387-2401.
[47]	BILGIN N, RICHTER A A, EHRENBERG M, et al. Ribosomal RNA and protein mutants resistant to spectinomycin[J]. EMBO J, 1990, 9(3):735-739.
[48]	BABA T, ARA T, HASEGAWA M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants:the Keio collection[J]. Mol Syst Biol, 2006, 2(1):2006. 0008.
[49]	LOZOVSKY E R, CHOOKAJORN T, BROWN K M, et al. Stepwise acquisition of pyrimethamine resistance in the malaria parasite[J]. Proc Natl Acad Sci U S A, 2009, 106(29):12025-12030.
[50]	LINDSEY H A, GALLIE J, TAYLOR S, et al. Evolutionary rescue from extinction is contingent on a lower rate of environmental change[J]. Nature, 2013, 494(7438):463-467.
[51]	REYNOLDS M G. Compensatory evolution in rifampin-resistant Escherichia coli[J]. Genetics, 2000, 156(4):1471-1481.
[52]	MACLEAN R C, PERRON G G, GARDNER A. Diminishing returns from beneficial mutations and pervasive epistasis shape the fitness landscape for rifampicin resistance in Pseudomonas aeruginosa[J]. Genetics, 2010, 186(4):1345-1354.
[53]	HALL A R, MACLEAN R C. Epistasis buffers the fitness effects of rifampicin- resistance mutations in Pseudomonas aeruginosa[J]. Evolution, 2011, 65(8):2370-2379.
[54]	SOLÉ M, FÀBREGA A, COBOS-TRIGUEROS N, et al. In vivo evolution of resistance of Pseudomonas aeruginosa strains isolated from patients admitted to an intensive care unit:mechanisms of resistance and antimicrobial exposure[J]. J Antimicrob Chemother, 2015, 70(11):3004-3013.
[55]	DALLINGER W H. The president's address[J]. J Roy Microsc Soc, 1887, 7(2):185-199.
[56]	KLIRONOMOS J N, ALLEN M F, RILLIG M C, et al. Abrupt rise in atmospheric CO2 overestimates community response in a model plant-soil system[J]. Nature, 2005, 433(7026):621-624.
[57]	JAHN L J, MUNCK C, ELLABAAN M M H, et al. Adaptive laboratory evolution of antibiotic resistance using different selection regimes lead to similar phenotypes and genotypes[J]. Front Microbiol, 2017, 8:816.
[58]	LOSOS J B. Convergence, adaptation, and constraint[J]. Evolution, 2011, 65(7):1827-1840.
[59]	ROSENBERG E Y, BERTENTHAL D, NILLES M L, et al. Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein[J]. Mol Microbiol, 2003, 48(6):1609-1619.
[60]	LIN D L, TRAN T, ALAM J Y, et al. Inhibition of aminoglycoside 6'-N-acetyltransferase type Ib by zinc:reversal of amikacin resistance in Acinetobacter baumannii and Escherichia coli by a zinc ionophore[J]. Antimicrob Agents Chemother, 2014, 58(7):4238-4241.
[61]	RODRÍGUEZ-VERDUGO A, GAUT B S, TENAILLON O. Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress[J]. BMC Evol Biol, 2013, 13(1):50.
[62]	ALLEN R C, PFRUNDER-CARDOZO K R, HALL A R. Collateral sensitivity interactions between antibiotics depend on local abiotic conditions[J]. mSystems, 2021, 6(6):e01055-21.
[63]	PODNECKY N L, FREDHEIM E G A, KLOOS J, et al. Conserved collateral antibiotic susceptibility networks in diverse clinical strains of Escherichia coli[J]. Nat Commun, 2018, 9(1):3673.

Bacterial Collateral Sensitivity:A New Perspective to Optimize Treatments

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 63

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	ZHOU Wenhui, BAO Hongxia, WANG Junhao, HUANG Yuanling, WANG Wenhui, HAO Haihong. Therapeutic Effect of Licorice Chalcone A in Combination with Three Antibiotics on Clostridium perfringens Infection in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(1): 334-345.
[2]	FAN Jinquan, ZHANG Yuhang, TANG Wuyang, ZHAO Xinyu, LI Pishun, ZHENG Xiaofeng. Inhibitory Effect of Decitabine on Porcine Circovirus Type 2 in vitro [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(12): 5134-5142.
[3]	LIANG Wuying, LIU Zhen, ZENG Yuqi, Lü Junjin, MO Ruiwen, YUAN Liguo. Effect of 1-methylhydantoin on Sodium Channel Nav1.8 in Rats with Chronic Pain [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(12): 5312-5317.
[4]	SHAN Qiang, WANG Xue, ZHU Yaohong, WANG Jiufeng. Application Prospect of Anti-inflammatory Mechanism of Lactobacillus rhamnosus and Its Prevention and Treatment in Livestock Diseases [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4537-4550.
[5]	WU Zhouhui, WANG Yu, DU Heng, WANG Zhiwen, XIAO Shuang, WU Jinliang, WANG Zhen. Analysis of the Antibacterial Sensitization Activity of Tirapazamine against Multi-Drug Resistant Salmonella [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(10): 4362-4371.
[6]	SUN Panpan, CAO Zhigang, LING Xiaoya, SUN Na, SUN Yaogui, LI Hongquan. Comparison of Anti-inflammatory Effects of Matrine Combined with Different Antibiotics [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(10): 4411-4421.
[7]	WANG Zhixia, BAI Lixia, QIN Zhe, LIU Xiwang, YANG Yajun, LI Shihong, GE Wenbo, LI Jianyong. Establishment and Validation of the Determination Method for the Related Substances in Aspirin Eugenol Ester Granules [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(8): 3500-3509.
[8]	WANG Ruijie, HONG Zhikai, DONG Yingjiao, CHEN Yao, WANG Jinyu, WANG Guanhua. Effect of Oxytetracycline and Andrographolide on the Metabolism of Chicken Intestinal Tracts Using UPLC-Q-TOF-MS/MS-based Metabolomic Approach [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(7): 3078-3090.
[9]	ZHANG Xiao, LI Dandan, TIAN Hongli, OU Chunmin, YANG Long, OUYANG Wuqing, ZHENG Yin. Alpha-pinene Is the Main Active Ingredient of Cacumen Platycladi against Trichophyton rubrum with ERG3 as Its Target [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(4): 1690-1702.
[10]	LIN Mengjuan, GAO Shasha, ZHAO Xingchen, ZHONG Yuxin, WU Jun, ZHANG Junren, GUO Dawei. Research Progress on Antiprotozoal Activity of Halofuginone [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 924-933.
[11]	CHEN Yang, WANG Yueli, CHEN Shiqi, LI Nanxin, ZHANG Wei, SHU Gang, XU Funeng, LI Haohuan, LIN Juchun, FU Hualin. Intestinal Absorption Characteristics of Florfenicol based on Oligopeptide Transporters [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 1240-1248.
[12]	YANG Yanbei, XU Jing, LIU Wanping, TAO Aini, FENG Yulin, SUN Yong, WANG Chuang, LIU Jian. Effects of Low-concentration Azitromycin on Protein Expression, Capsular Polysaccharides and Drug Susceptibility of Streptococcus suis Type 2 [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(2): 757-765.
[13]	HONG Mian, HUANG Jiamin, CHEN Dongmei, XIE Shuyu. Research Progress of Nanotechnology to Enhance Antibacterial Efficacy of Antibacterial Drugs [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 3731-3736.
[14]	LIU Xu, PAN Yinchuan, YANG Yajun, LIU Xiwang, MA Ning, LI Jianyong. Inhibiting Effect of Aspirin Eugenol Ester on Lipopolysaccharide-induced Inflammatory Response in Mouse Macrophages in vitro [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 4048-4057.
[15]	SUN Dong, QU Sha, LI Xuan, TANG Shanhu, LI Sining, HAO Gang. Comparative Study on the Membrane Action Mechanism of Tachyplesin Ⅰ and Its Analogue on Escherichia coli [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(9): 3180-3189.