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Quorum Sensing Inhibition: A Target for Treating Chronic Wounds

  • Lahari Das
  • Yogendra Singh
Chapter

Abstract

Chronic wounds are serious medical problem which sometimes become fatal. Bacterial infections are one of the major causes for chronic wounds and delay in their healing. Pathogenic bacteria form biofilms on the surface of wounds. Biofilms are organized polymicrobial structures where bacteria are encased in exopolysaccharide layer and are present in metabolically quiescent state, thus making the wounds resistant to antimicrobial treatment. This delays the wound healing process by slowing down tissue repair and by inducing chronic inflammation at the site of the wound. The cell to cell communication system also known as the quorum sensing (QS) system is required for biofilm formation and coordinated virulence activities. QS inhibitors have emerged as important candidates for inhibiting biofilm formation, maintenance and expression of virulence factors. Use of these compounds alone or in combination with antibiotics may aid in rapid healing of chronic wounds and tissue regeneration. This chapter focuses on the role of QS in chronic wounds and the use of QS inhibitors for treating such wounds and facilitating wound healing.

Keywords

Chronic wounds Wound healing Quorum sensing Biofilms Antibiotic resistance Quorum sensing inhibitors 

References

  1. Abbas H, Shaldam MA (2016) Glyceryl trinitrate is a novel inhibitor of quorum sensing in Pseudomonas aeruginosa. Afr Health Sci 16:1109–1117.  https://doi.org/10.4314/ahs.v16i4.29
  2. Agarwala M, Choudhury B, Yadav RN (2014) Comparative study of antibiofilm activity of copper oxide and iron oxide nanoparticles against multidrug resistant biofilm forming uropathogens. Indian J Microbiol 54:365–368.  https://doi.org/10.1007/s12088-014-0462-z CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ahiwale SS, Bankar AV, Tagunde S, Kapadnis BP (2017) A bacteriophage mediated gold nanoparticle synthesis and their anti-biofilm activity. Indian J Microbiol 57:188–194.  https://doi.org/10.1007/s12088-017-0640-x CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arasu MV, Al-Dhabi NA, Rejiniemon TS, Lee KD, Huxley VAJ, Kim DH, Duraipandiyan V, Karuppiah P, Choi KC (2015) Identification and characterization of Lactobacillus brevis P68 with antifungal, antioxidant and probiotic functional properties. Indian J Microbiol 55:19–28.  https://doi.org/10.1007/s12088-014-0495-3 CrossRefGoogle Scholar
  5. Arya AK, Tripathi R, Kumar S, Tripathi K (2014) Recent advances on the association of apoptosis in chronic non healing diabetic wound. World J Diabetes 5:756–762.  https://doi.org/10.4239/wjd.v5.i6.756 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Beaufort N, Corvazier E, Mlanaoindrou S, de Bentzmann S, Pidard D (2013) Disruption of the endothelial barrier by proteases from the bacterial pathogen Pseudomonas aeruginosa: implication of matrilysis and receptor cleavage. PLoS One 8:e75708.  https://doi.org/10.1371/journal.pone.0075708 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Begum IF, Mohankumar R, Jeevan M, Ramani K (2016) GC–MS analysis of bioactive molecules derived from ParacoccuspantotrophusFMR19 and the antimicrobial activity against bacterial pathogens and MDROs. Indian J Microbiol 56:426–432.  https://doi.org/10.1007/s12088-016-0609-1 CrossRefGoogle Scholar
  8. Bjarnsholt T, Ciofu O, Molin S, Givskov M, Hoiby N (2013) Applying insights from biofilm biology to drug development - can a new approach be developed? Nat Rev Drug Discov 12:791–808.  https://doi.org/10.1038/nrd4000 CrossRefPubMedGoogle Scholar
  9. Bose D, Chatterjee S (2015) Antibacterial activity of green synthesized silver nanoparticles using Vasaka (Justiciaadhatoda L.) leaf extract. Indian J Microbiol 55:163–167.  https://doi.org/10.1007/s12088-015-0512-1 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brackman G, Coenye T (2015) Quorum sensing inhibitors as anti-biofilm agents. Curr Pharmaceutical Ddesign 21:5–11. doi: Not availableGoogle Scholar
  11. Castillo-Juarez I, Maeda T, Mandujano-Tinoco EA, Tomas M, Perez-Eretza B, Garcia-Contreras SJ, Wood TK, Garcia-Contreras R (2015) Role of quorum sensing in bacterial infections. World J Clinic Cases 3:575–598.  https://doi.org/10.12998/wjcc.v3.i7.575 CrossRefGoogle Scholar
  12. Clinton A, Carter T (2015) Chronic wound biofilms: pathogenesis and potential therapies. Lab Med 46:277–284.  https://doi.org/10.1309/LMBNSWKUI4JPN7SO CrossRefPubMedGoogle Scholar
  13. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg, EP (1998) Theinvolvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298. doi:Not availableGoogle Scholar
  14. De Ryck T, Vanlancker E, Grootaert C, Roman BI, De Coen LM, Vandenberghe I, Stevens CV, Bracke M, Van de Wiele T, Vanhoecke B (2015) Microbial inhibition of oral epithelial wound recovery: potential role for quorum sensing molecules? AMB Express 5:27.  https://doi.org/10.1186/s13568-015-0116-5 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dobrucka R, Długaszewska J (2015) Antimicrobial activities of silver nanoparticles synthesized by using water extract of Arnicae anthodium. Indian J Microbiol 55:168–174.  https://doi.org/10.1007/s12088-015-0516-x CrossRefPubMedPubMedCentralGoogle Scholar
  16. Eming SA, Kaufmann J, Lohrer R, Krieg T (2007) Chronic wounds. Novel approaches in researchand therapy. Hautarzt 58:939–944.  https://doi.org/10.1007/s00105-007-1402-1 CrossRefPubMedGoogle Scholar
  17. Forster AJ, Oake N, Roth V, Suh KN, Majewski J, Leeder C, van Walraven C (2013) Patient-level factors associated with methicillin-resistant Staphylococcus aureus carriage at hospital admission: a systematic review. Am J Inf Cntrol 41:214–220.  https://doi.org/10.1016/j.ajic.2012.03.0 CrossRefGoogle Scholar
  18. Gama JA, Abby SS, Vieira-Silva S, Dionisio F, Rocha EP (2012) Immune subversion andquorum-sensing shape the variation in infectious dose among bacterial pathogens. PLoS Pathog 8:e1002503.  https://doi.org/10.1371/journal.ppat.1002503 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Garcia-Contreras R (2016) Is quorum sensing interference a viable alternative to treat Pseudomonas aeruginosa infections? Front Microbiol 7:1454.  https://doi.org/10.3389/fmicb.2016.01454 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gonzalez AC, Costa TF, Andrade ZA, Medrado AR (2016) Wound healing – a literature review. Anais Brasileiros de Dermat 91:614–620.  https://doi.org/10.1590/abd1806-4841.20164741 CrossRefGoogle Scholar
  21. Gui Z, Wang H, Ding T, Zhu W, Zhuang X, Chu W (2014) Azithromycin reduces the production of α-hemolysin and biofilm formation in Staphylococcus aureus. Indian J Microbiol 54:114–117.  https://doi.org/10.1007/s12088-013-0438-4 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Guo S, Dipietro LA (2010) Factors affecting wound healing. J Dental Res 89:219–229.  https://doi.org/10.1177/0022034509359125 CrossRefGoogle Scholar
  23. Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453:314–321.  https://doi.org/10.1038/nature07039 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Haji Zaine N, Burns J, Vicaretti M, Fletcher JP, Begg L, Hitos K (2014) Characteristics of diabetic foot ulcers in Western Sydney, Australia. J Foot Ankle Res 7:39.  https://doi.org/10.1186/s13047-014-0039-4 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hocking AM (2015) The role of chemokines in mesenchymal stem cell homing to wounds. Adv Wound Care 4:623–630.  https://doi.org/10.1089/wound.2014.0579 CrossRefGoogle Scholar
  26. Hong WX, Hu MS, Esquivel M, Liang GY, Rennert RC, McArdle A, Paik KJ, Duscher D, Gurtner GC, Lorenz HP (2014) The role of hypoxia-inducible factor in wound healing. Adv Wound Care 3:390–399.  https://doi.org/10.1089/wound.2013.0520 CrossRefGoogle Scholar
  27. Huma N, Shankar P, Kushwah J, Bhushan A, Joshi J, Mukherjee T, Raju SC, Purohit HJ, Kalia VC (2011) Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21:1001–1011.  https://doi.org/10.4014/jmb.1105.05056 CrossRefPubMedPubMedCentralGoogle Scholar
  28. James GA, Swogger E, Wolcott R, Pulcini E, Secor P, Sestrich J, Costerton JW, Stewart PS (2008) Biofilms in chronic wounds. Wound Repair Regen 16:37–44.  https://doi.org/10.1111/j.1524-475X.2007.00321.x CrossRefPubMedGoogle Scholar
  29. Jeyanthi V, Velusamy P (2016) Anti-methicillin resistant Staphylococcus aureus compound isolation from halophilic Bacillus amyloliquefaciensMHB1 and determination of its mode of action using electron microscope and flow cytometry analysis. Indian J Microbiol 56:148–157.  https://doi.org/10.1007/s12088-016-0566-8 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245.  https://doi.org/10.1016/j.biotechadv.2012.10.00 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kalia VC (2014a) Microbes, antimicrobials and resistance: the battle goes on. Indian J Microbiol 54:1–2.  https://doi.org/10.1007/s12088-013-0443-7 CrossRefPubMedCentralGoogle Scholar
  32. Kalia VC (2014b) In search of versatile organisms for quorum-sensing inhibitors: acyl homoserinelactones (AHL)-acylase and AHL-lactonase. FEMS Microbiol Letts 359:143.  https://doi.org/10.1111/1574-6968.12585 CrossRefGoogle Scholar
  33. Kalia VC (2015a) Quorum sensing vs quorum quenching: a battle with no end in sight. In: Kalia VC (ed). Springer India, New Delhi. http://link.springer.com/book/10.1007/978-81-322-1982-8 Google Scholar
  34. Kalia VC (2015b) Microbes: the most friendly beings?In: Kalia VC (ed) Quorum sensing vs quorum quenching: A battle with no end in sight. Springer India, New Delhi, pp 1–5. doi: https://doi.org/10.1007/978-81-322-1982-8_1 CrossRefGoogle Scholar
  35. Kalia VC, Kumar P (2015a) Potential applications of quorum sensing inhibitors in diverse fields. In: Kalia VC (ed) Quorum sensing vs Quorum quenching: a battle with no end in sight. Springer India, New Delhi, pp 359–370. doi: https://doi.org/10.1007/978-81-322-1982-8_29 CrossRefGoogle Scholar
  36. Kalia VC, Kumar P (2015b) The battle: Quorum-sensing inhibitors versus evolution of bacterialresistance. In: Kalia VC (ed) Quorum sensing vs Quorum quenching: a battle with no end in sight. Springer India, New Delhi, pp 385–391. doi: https://doi.org/10.1007/978-81-322-1982-8_31 CrossRefGoogle Scholar
  37. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drugtargets. Critic Rev Microbiol 37:121–140.  https://doi.org/10.3109/1040841X.2010.532479 CrossRefGoogle Scholar
  38. Kalia VC, Raju SC, Purohit HJ (2011) Genomic analysis reveals versatile organisms for quorumquenching enzymes: acyl-homoserine lactone-acylase and lactonase. Open Microbiol J 5:1–13.  https://doi.org/10.2174/1874285801105010001 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kalia VC, Wood TK, Kumar P (2014a) Evolution of resistance to quorum-sensing inhibitors. Microb Ecol 68:13–23.  https://doi.org/10.1007/s00248-013-0316-y CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kalia VC, Kumar P, Pandian SK, Sharma P (2014b) Biofouling control by quorum quenching. In: Kim SK (ed) Hb_25 Springer handbook of marine biotechnology chapter 15. Springer, Berlin, pp 431–440CrossRefGoogle Scholar
  41. Kalia VC, Prakash J, Koul S, Ray S (2017) Simple and rapid method for detecting biofilm formingbacteria. Indian J Microbiol 57:109–111.  https://doi.org/10.1007/s12088-016-0616-2 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Keays T, Ferris W, Vandemheen KL, Chan F, Yeung SW, Mah TF, Ramotar K, Saginur R, Aaron SD (2009) A retrospective analysis of biofilm antibiotic susceptibility testing: a betterpredictor of clinical response in cystic fibrosis exacerbations. J Cystic Fibrosis 8:122–127.  https://doi.org/10.1016/j.jcf.2008.10.005 CrossRefGoogle Scholar
  43. Khanh VC, Ohneda K, Kato T, Yamashita T, Sato F, Tachi K, Ohneda O (2017) Uremic toxins affectthe imbalance of redox state and overexpression of prolyl hydroxylase 2 inhumanadipose tissue-derived mesenchymal stem cells involved in wound healing. Stem Cells Dev 26:948–963.  https://doi.org/10.1089/scd.2016.0326 CrossRefPubMedGoogle Scholar
  44. Kim HK, Missiakas D, Schneewind O (2014) Mouse models for infectious diseases caused by Staphylococcus aureus. J Immunol Methods 410:88–99.  https://doi.org/10.1016/j.jim.2014.04.007 CrossRefPubMedGoogle Scholar
  45. Kong W, Liang H, Shen L, Duan K (2009) Regulation of type III secretion system by Rhl and PQS quorum sensing systems in Pseudomonas aeruginosa. Acta Microbiol Sin 49:1158–1164Google Scholar
  46. Koul S, Kalia VC (2017) Multiplicity of quorum quenching enzymes: a potential mechanism to limitquorum sensing bacterial population. Ind J Microbiol 57:100–108.  https://doi.org/10.1007/s12088-016-0633-1 CrossRefGoogle Scholar
  47. Koul S, Prakash J, Mishra A, Kalia VC (2016) Potential emergence of multi-quorum sensinginhibitor resistant (MQSIR) bacteria. Indian J Microbiol 56:1–18.  https://doi.org/10.1007/s12088-015-0558-0 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kumar P, Patel SKS, Lee JK, Kalia VC (2013) Extending the limits of Bacillus for novelbiotechnological applications. Biotechnol Adv 31:1543–1561.  https://doi.org/10.1016/j.biotechadv.2013.08.007 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kumar P, Koul S, Patel SKS, Lee JK, Kalia VC (2015) Heterologous expression of quorum sensinginhibitory genes in diverse organisms. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battlewith no end in sight. Springer India, New Delhi, pp 343–356. doi: https://doi.org/10.1007/978-81-322-1982-8_28 CrossRefGoogle Scholar
  50. LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111.  https://doi.org/10.1128/MMBR.00046-12 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lejeune P (2003) Contamination of abiotic surfaces: what a colonizing bacterium sees and how to blur it. Trends Microbiol 11:179–184.  https://doi.org/10.1016/S0966-842X(03)00047-7 CrossRefPubMedGoogle Scholar
  52. Li J, Chen J, Kirsner R (2007) Pathophysiology of acute wound healing. Clin Dermatol 25:9–18.  https://doi.org/10.1016/j.clindermatol.2006.09.007 CrossRefPubMedGoogle Scholar
  53. Maeda T, Garcia-Contreras R, Pu M, Sheng L, Garci LR, Tomas M, Wood TK (2012) Quorum quenching quandary: resistance to antivirulence compounds. ISME J 6:493–501.  https://doi.org/10.1038/ismej.2011.122 CrossRefPubMedGoogle Scholar
  54. Maxson S, Lopez EA, Yoo D, Danilkovitch-Miagkova A, Leroux MA (2012) Concise review: role of mesenchymal stem cells in wound repair. Stem Cells Trans Med 1:142–149.  https://doi.org/10.5966/sctm.2011-0018 CrossRefGoogle Scholar
  55. Medrado AR, Pugliese LS, Reis SR, Andrade ZA (2003) Influence of low level laser therapy on wound healing and its biological action upon myofibroblasts. Lasers Surg Med 32:239–244.  https://doi.org/10.1002/lsm.10126 CrossRefPubMedGoogle Scholar
  56. Medrado A, Costa T, Prado T, Reis S, Andrade Z (2010) Phenotype characterization of pericytes during tissue repair following low-level laser therapy. Photodermatol Photoimmunol Photomed 26:192–197.  https://doi.org/10.1111/j.1600-0781.2010.00521.x CrossRefPubMedGoogle Scholar
  57. Menke NB, Ward KR, Witten TM, Bonchev DG, Diegelmann RF (2007) Impaired wound healing. Clin Dermatol 25:19–25.  https://doi.org/10.1016/j.clindermatol.2006.12.005 CrossRefPubMedGoogle Scholar
  58. Nayak BS, Sandiford S, Maxwell A (2009) Evaluation of the wound-healing activity of ethanolicextract of Morinda citrifolia L. leaf. Evid Compl Alter Med 6:351–356.  https://doi.org/10.1093/ecam/nem127 CrossRefGoogle Scholar
  59. Nishifuji K, Sugai M, Amagai M (2008) Staphylococcal exfoliative toxins: “molecular scissors” of bacteria that attack the cutaneous defense barrier in mammals. J Dermatol Sci 49:21–31.  https://doi.org/10.1016/j.jdermsci.2007.05.007 CrossRefPubMedGoogle Scholar
  60. Omar A, Wright JB, Schultz G, Burrell R, Nadworny P (2017) Microbial biofilms and chronicwounds. Microorganisms 5:9.  https://doi.org/10.3390/microorganisms5010009 CrossRefPubMedCentralGoogle Scholar
  61. Oppenheimer-Shaanan Y, Steinberg N, Kolodkin-Gal I (2013) Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol 21:594–601.  https://doi.org/10.1016/j.tim.2013.08.005 CrossRefPubMedGoogle Scholar
  62. Reuter K, Steinbach A, Helms V (2016) Interfering with bacterial quorum sensing. Persp Med Chem 8:1–15.  https://doi.org/10.4137/PMC.S13209 CrossRefGoogle Scholar
  63. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilitiesfor its control. Cold Spring Harbor Perspect Med 2:pii:a012427. doi: https://doi.org/10.1101/cshperspect.a012427 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sana TG, Hachani A, Bucior I, Soscia C, Garvis S, Termine E, Engel J, Filloux A, Bleves S (2012) The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J Biol Chem 287:27095–27105.  https://doi.org/10.1074/jbc.M112.376368 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Saurav K, Costantino V, Venturi V, Steindler L (2017) Quorum sensing inhibitors from the sea discovered using bacterial N-acyl-homoserine lactone-based biosensors. Mar Drugs 15. doi:  https://doi.org/10.3390/md15030053 CrossRefPubMedCentralGoogle Scholar
  66. Serra R, Grande R, Butrico L, Rossi A, Settimio UF, Caroleo B, Amato B, Gallelli L, de Franciscis S (2015) Chronic wound infections: the role of Pseudomonas aeruginosa and Staphylococcus aureus. Expert Rev Anti-Infect Ther 13:605–613.  https://doi.org/10.1586/14787210.2015.1023291 CrossRefPubMedGoogle Scholar
  67. Sharma R, Jangid K (2015) Fungal Quorum sensing inhibitors. In: Kalia VC (ed) Quorum sensing vs Quorum quenching: a battle with no end in sight. Springer India, New Delhi, pp 237–257Google Scholar
  68. Sharma A, Lal R (2017) Survey of (Meta) genomic approaches for understanding microbial community dynamics. Indian J Microbiol 57:23–38.  https://doi.org/10.1007/s12088-016-0629-x CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122:3209–3213.  https://doi.org/10.1242/jcs.031187 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Shiva Krishna P, Sudheer Kumar B, Raju P, Murty MSR, Prabhakar Rao T, Singara Charya MA, Prakasham RS (2015) Fermentative production of pyranone derivate from marine Vibrio sp. SKMARSP9: isolation, characterization and bioactivity evaluation. Indian J Microbiol 55:292–301.  https://doi.org/10.1007/s12088-015-0521-0 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Siddiqui MF, Rzechowicz M, Harvey W, Zularisam AW, Anthony GF (2015) Quorum sensing based membrane biofouling control for water treatment: a review. J Water Proc Eng 30:112–122.  https://doi.org/10.1016/j.jwpe.2015.06.003 CrossRefGoogle Scholar
  72. Simonetti O, Cirioni O, Cacciatore I, Baldassarre L, Orlando F, Pierpaoli E, Lucarini G, Orsetti E, Provinciali M, Fornasari E (2016) Efficacy of the quorum sensing inhibitor FS10alone and in combination with Tigecycline in an animal model of Staphylococcal infected wound. PLoS One 11:e0151956.  https://doi.org/10.1371/journal.pone.0151956 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Szweda P, Gucwa K, Kurzyk E, Romanowska E, Dzierżanowska-Fangrat K, Jurek AZ, Kuś PM, Milewski S (2015) Essential oils, silver nanoparticles and propolis as alternative agents against fluconazole resistant Candida albicans, Candida glabrata and Candida krusei clinical isolates. Indian J Microbiol 55:175–183.  https://doi.org/10.1007/s12088-014-0508-2 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Thuraisingam T, Xu YZ, Eadie K, Heravi M, Guiot MC, Greemberg R, Gaestel M, Radzioch D (2010) MAPKAPK-2 signaling is critical for cutaneous wound healing. J Invest Dermatol 130:278–286.  https://doi.org/10.1038/jid.2009.209 CrossRefPubMedGoogle Scholar
  75. Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345–R353.  https://doi.org/10.1152/ajpregu.00454.2004 CrossRefPubMedGoogle Scholar
  76. Wadhwani SA, Shedbalkar UU, Singh R, Vashisth P, Pruthi V, Chopade BA (2016) Kinetics of synthesis of gold nanoparticles by Acinetobacter sp. SW30 isolated from environment. Indian J Microbiol 56:439–444.  https://doi.org/10.1007/s12088-016-0598-0 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Wilke GA, Bubeck Wardenburg J (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Natl Acad Sci U S A 107:13473–13478.  https://doi.org/10.1073/pnas.1001815107 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Lahari Das
    • 1
  • Yogendra Singh
    • 2
    • 3
  1. 1.Department of ZoologyUniversity of Delhi North CampusDelhiIndia
  2. 2.Department of ZoologyUniversity of DelhiDelhiIndia
  3. 3.Academy of Scientific & Innovative Research (AcSIR)New DelhiIndia

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