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9 Bacteriophages asBiocontrol Agents ofBiolm Infections Associated withAbiotic Prosthetic Devices
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9.5.3 Phage Therapy, Phage Cocktails, andCotherapy
Phage therapy for biolms is usually carried out by direct application over the biolm formed on the abiotic prosthetic device surface. Factors affecting biolm clearance success in direct applications include phage dosage, route of administration as well as the stage of biolm maturation and its resident clinical species [16,
76, 77]. Phage cocktails (combination of phage
with varying host specicities) have also proved very efcacious in controlling polymicrobial infections on abiotic prosthetic devices [78]. Medical applications of phage therapy have undergone clinical trials as in the case of phage burn (funded by European commission), a phage cocktail targeting Ps. aeruginosa and E. coli infections associated with burn patients [20].
Use of phages alongside sub-minimum inhib­itory concentrations of antibiotics in solution or in an immobilized form have been shown to be efcacious in controlling mature biolms [79,
80]. Meropenem-phage and amikacin-phage
combination showed synergistic activity in reducing planktonic and biolm formed Ps. aeruginosa biolms [81]. Phage antibiotic syn- ergistic treatment for Ps. aeruginosa PA14 bio­lm was tested with phage and 5 different bactericidal antibiotics [82].
9.5.4 Phage Enzybiotics
Phage-derived products such as bacteriolytic enzymes: lysins, depolymerases, as well biolm exopolymeric matrix degrading enzymes are being exploited as anti-biolm agents while cir­cumventing potential threats associated with the use of live phages [83, 84]. Engineered bacterio­phage enzymes have been employed to disperse biolms by breaking down components of the extracellular polymeric matrix [85]. These phage- derived endolysins, including the novel Artilysins, show activity against persister cells of gram- positive, gram-negative, as well Mycobacterial origin [86]. The T7 phage was
genetically engineered to express the dsp B gene encoding biolm­Acinobacillus actinomycetemcomitans which drastically reduced E. coli biolm counts even as such enzymes have low substrate specicities [87]. Use of T7-engineered phages expressing quorum sensing quenching enzymes AiiA lac­tonase effectively inhibited mixed biolm of Ps. aeruginosa and E.coli [88]. S. aureus biolm control with the use of a chimeric protein CHAPSH3b derived from peptidoglycan hydro­lase of phage vB_SauS-philPLA88 and lyso­staphin was reported [ with cellulose- binding module for facilitating phage on wound dressings and retained antimi­crobial activity against E. coli and Micrococcus lysodeikticus bacteria [90].
dispersing enzymes from
89].T4 lysozyme is fused
9.5.5 Phage Directly Aecting Antibiotic Resistance within theBiolm
Antibiotic resistance is one of the major problems of biolm-associated prosthetic device infections. Isolation of phages that exert selective pressure on bacteria to confer them sensitive to the current regimen of antibiotics is a new strategy in phage biocontrol. A lytic bacteriophage OMKO1 (fam­ily Myoviridae) of Pseudomonas aeruginosa that utilizes the outer membrane porin M (OprM) of the multidrug efux systems MexAB and MexXY as a receptor-binding site has been isolated [91]. Phage-OMKO1-resistant strain (oprM knockout) showed increased sensitivity to ceftazidime, cip­rooxacin, tetracycline, and erythromycin antibi­otics. A novel method of introducing antibiotic sensitizing gene cassette through genes rpsL and gyrA to two antibiotics, streptomycin and nali­dixic acid, respectively, through temperate phage therapy to reverse engineer antibiotic resistance in E. coli pathogens is reported [92]. Gene transfer of antibiotic resistance genes through conjugative plasmids has higher frequency rates within the closely conned populations within the biolm. A lytic plasmid- dependant phage PRD1 and antibiotic- resistant plasmid RP4 co-evolution was
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studied in E. coli and Salmonella enteric. Infections with PRD1 drastically reduced the fre­quency of antibiotic resistance cells [93]. Bacteriophages could play a signicant role in restricting the spread of plasmid-encoded antibi­otic resistance [94].
9.5.6 Overcoming Bacterial Phage Defense Systems andCRISPR­Dependent Biolm Inhibition
Development of resistance to phage infections by the host may result in ineffective biolm control. Bacterial cells may acquire resistance either by altering phage entry receptors or through viral nucleic acid degradation post entry via the CRISPR (Clustered regularly interspaced short palindromic repeats) and CRISPR-associated Cas9 cascade proteins [69, 95]. CRISPR are pro­karyotic adaptive immune systems which involve an array of repetitive sequences with spacers acquired from potential foreign DNA sources such as viruses, plasmids, or transposons. Upon reinfection with foreign DNA source, CRISPR RNA (crRNA) activates Cas proteins to degrade the complimentary foreign DNA.
Bacteriophages in response encode anti CRISPR proteases that inhibit the CRIPR defense system [96]. Genetically engineered phages that encode anti CRISPR proteases have been designed. Pseudomonas DMS3 temperate phage through elegant experiments involving the CRIPR Cas system was shown to modulate bio­lm formation and swarming motility behavior [97]. In Streptococcus thermophilus phages mutations within the protospacer regions provide protection against CRISPR cas system. In Vibrio cholera phage-encoded CRISPR/Cas system is used to counteract a phage inhibitory chromo­somal island of the bacterial host. A recent study describes a novel Bacteriophage extrusion (BREX) system which involves a six cassette gene system in Bacillus subtilis wherein host DNA is methylated at fth position of a non­palindromic 5-TAGGAC-3 hexamer sequence and phage inhibited by blocking phage DNA rep­lication of both lytic and temperate phages [98].
Phage-transferable CRISPR-Cas systems are capable of specically killing pathogens or resen­sitizing them to antibiotics [
69, 99].
9.5.7 Phages andQuorum Sensing
In a recent work, it was shown that phage phiCDHM1 infecting Clostridium difcile har­bors QS gene homologs (agr3) which can inu­ence pathogen behavior [100]. The decision between lytic and lysogenic behavior of phage infection is also shown to be guided by arbitrium system which consists of the production of oligo­meric signaling peptides [101]. Understanding phage communication signals can help better manipulate biolm dispersal strategies using phage therapy. Engineered T7 phages expressing quorum quenching molecules lactonases have successfully inhibited Ps. aeruginosa and E. coli biolm [88].
9.5.8 Phages asTheranostics
Theranostics combines specic targeted therapy wherein diagnosis and therapy are combined in a single agent [102]. Classical phage typing involv­ing the use of specic phages for bacterial strain identication has now been extended to the use of phages as biosensors or diagnostic markers [20]. Fluorescent-labeled Mycobacteriophage DS6A can differentiate between members of MTB com­plex [103]. NanoLuc reporter phage has been developed for the detection of E. coli OH:157 foodborne pathogen [104]. Similar technological advances can be applied for the diagnosis as well as therapy of DRI-associated biolms.
9.5.9 Phages asVaccine Delivery Agents
Prophylactic measures using phage nanosystems used as vaccine-carrying agents prior to a planned implantation for the prevention of bio­lm formation by common skin microora or nosocomial infections are being explored [75]. A
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combination of phage display vaccines and phage DNA vaccines are being developed wherein antigens as fusion products are expressed on the major surface proteins of phages such as M13 and T4 phages while it car­ries gene for vaccine candidate in its genome under a strong expression promoter [105].
9.6 Control ofBiolm­Associated DRI withPhage Applications
Applications of the above phage control strate­gies are being successfully applied for the mitiga­tion of biolm-related infections on medical implants in invitro studies, animal models, and human therapies. The control of catheter-induced urinary tract infections (CAUTI) caused by invitro-induced Proteus mirabilis biolms with two novel virulent phages, the podovirus vB_ PmiP_5460 and the myovirus vB_PmiM_5461 was reported [106]. Further, phage-coated cathe­ters using a dynamic biolm model simulating CAUTIs showed a signicant reduction of P. mirabilis biolm formation up to 168h of cathe­terization [106]. The potential of a 3 phage cock­tail in treatment of established infection as well as early colonization of invitro model of cathe­terized urinary tract infection showed signicant decrease in crystalline biolm formation [107]. Another study investigated the effect of pretreat­ing hydrogel-coated silicone catheters with mix­tures of mixed species (Pseudomonas aeruginosa and Proteus mirabilis) bacteriophages on the development of single- and two-species biolms in a multiday continuous-ow in vitro model using articial urine media. Phage pretreatment reduced P. aeruginosa biolm counts by 4 log10 CFU/cm2 (P ≤ 0.01) and P. mirabilis biolm counts by >2 log10 CFU/cm2 (P ≤ 0.01) over 48h [108].
Catheter-related bloodstream infections (CRBSI) are indicative in patients requiring long­term treatment of parenteral nutrition, chemo­therapy, or hemodialysis [60]. Antibiotic lock therapy (ALT) is a catheter sterilization method using high concentrations of antibiotics into the
catheter lumen for extended periods of time. In a rabbit model, treatment of 24-h S. aureus biolm­infected central venous catheters with a S. aureus­specic bacteriophage K antimicrobial-lock technique signicantly reduced S. aureus bacte­rial colonization and biolm presence [109].
2
Mean colony-forming units (CFU/ cm
) of bio­lm measured in the distal catheter segment were signicantly decreased in experimental animals (7.6×103CFU/cm2) as compared with controls (1.2×105CFU/cm2). Scanning electron micros­copy demonstrated that biolms were present on the surface of ve of ve control catheters but only one of ve treated catheters (P=0.048).
In catheter-induced aortic vegetation and experimental endocarditis due to Ps. aeruginosa biolm studied in Wistar rats, synergistic action between intravenous supply of phage cocktail and antibiotic ciprooxacin reduced bacterial load in comparison to control [90]. Synergistic activity of phage and antibiotic combination has proved to be highly effective in controlling antibiotic- resistant biolms. In vitro brin clots as well as aorta-induced experimental endocardi­tis treated with phage/ciprooxacin combina­tions were highly synergistic, killing >6 log CFUs/g of vegetations in 6 h and successfully treating 64% (n=7/11) of rats in comparison to single-dose phage therapy or ciprooxacin mono treatments that killed 2.5 log CFUs/g of vegeta­tions in 6h (P<0.001 vs. untreated controls) .
Prosthetic joint infections (PJI) are a devastat­ing postsurgical complication [46]. S. aureus bio- lms account for 20–40% arthoplasty infections following knee or hip joint replacements leading to prolonged antibiotic treatments, multiple sur­geries, and replacement of prosthetics or eventual amputations. The use of engineered bacterio­phages targeting S. aureus and other microbial infections has been successfully demonstrated in the following studies. In an implant-related infec­tion model in rats, MRSA and Pseudomonas aeruginosa-specic bacteriophages were tested with antibiotic regimen of teicoplanin for MRSA and imipenem, cilastatin, and amikacin for Ps. aeruginosa, respectively [110]. S. aureus-specic phage along with linezolid (incorporated in hydroxymethyl propyl cellulose biopolymer)
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allowed gradual release of the two agents at the implant site in a mouse model of prosthetic joint infection with S. aureus ATCC 43300(MRSA) resulting in reduction in bacterial adherence as well inammation [111].
Bacteriophage treatments in face of chronic symptomatic antibiotic-resistant infections have also been implicated in having anti-inamma­tory properties [112]. In a clinical study, thirty­seven patients, some with periprosthetic infections with chronic antibiotic-resistant bac­terial infections, were treated with oral bacterio­phage therapy and their inammation markers such as C reactive protein and mean WBC were found to diminish [112].
9.7 Outlooks andChallenges
Biolm infections of prosthetic devices not only cause inammatory responses but also lead to complications due to loosening of implanted devices, wound dehiscence, or disruption of pros­thetic valves and embolism. Bacteriophage ther­apy is a promising alternative to counter effects of recalcitrant biolms and several phage strate­gies have been described for the control of infec­tious microorganisms. Even so, specic study targeting their behavior with biolms is still being explored. Some of the greatest challenges that phages face within the biolm are penetra­tion through the exopolymeric substances (EPS) which is being hopefully addressed with several genetically engineered phages expressing lysins and EPS degrading enzymes. Even within bio­lms, the presence of multiple species is com­mon and hence the use of broad range phages is required for effective biolm removal [113]. A host range expansion protocol wherein cocultur­ing of several Ps. aeruginosa cultures with four phage mix was used to develop a phage cocktail with the requisite host range [114]. Two sequen­tial multihost strategies have been evolved for the isolation of polyvalent bacteriophages PX1 of the Podoviridae family and PEf1 of the Siphoviridae family using Pseudomonas putida F1 or Escherichia coli K-12 and subsequently used to infect model problematic bacteria [115].
Phage dosing for biolms clearance on pros­thetic devices is very critical. Initial high dose of phage application when bacterial density is high results in an immediate arrest of biolm growth. However, if there is low bacterial density, initial phage concentrations may decay as a conse­quence of lack of adequate host supply [ Slow release of appropriate dosages of phages using phage encapsulation technology can be used to maintain in situ phage amplication in response to microbe within the biolm [117,
118].
Immune response to phage administered is still of concern in human phage therapy and stud­ies documenting humoral responses to phages have been recorded [ Pseudomonas phages F8 and T4in mice showed an upregulation of innate (phagocytes) and spe­cic immune response (antibodies) to the circu­lating phages similar to that observed for eukaryotic viruses [120]. Mathematical modeling of the experimental data also showed that preim­munization or natural pre-exposure to a phage may hamper its effectiveness as a therapeutic agent.
Use of biolm-dispersing agents in co-therapy approaches or the use of genetically engineered phages expressing dispersive enzymes, nitric oxides, and quorum sensing antagonists is effec­tive in targeting biolms [68, 87]. Following a biolm-dispersive regimen, the use of antimicro­bial agents at much lower inhibitory concentra­tions appears to be a comprehensive antibiolm strategy.
Detection of biolms remains one of the great­est challenges of biolm infections [5]. New molecular methods should be introduced in the practice along with microscopy which can sub­stantially reduce time taken in conventional cul­ture methods [4]. These innovative methods are expected to provide a more sensitive bacterial enumeration and detection that would contribute to better treatment regimens. Phage theranostics combine diagnosis and therapeutic applications for effective and timely control of biolm­associated device-related infections [102].
Apart from preventing infections on pros­thetic devices, bacteriophages are also nding
119]. Immune response to
116].
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use in regenerative medicine as nanoscaffolds for tissue regeneration [20]. Genetically engi­neered M13 phages have long rod-shaped nano­structures which self-assemble as scaffolds used for tissue regeneration [71]. Additionally, the M13 major coat protein can be genetically engineered to express cellular differentiating markers helping in osteogenesis and neovascu­larization. Phage- based regenerative medicine shows great promise with developing technolo­gies such as 3D printing and precision-based nanomedicines [20].
Since there is currently no legislation regard­ing the use of bacteriophage therapy, the develop­ment of bacteriophages as novel drugs comes under the purview of the Food and Drug Administration (FDA) in the United States. Similarly the efcacy of phage therapy is yet not approved by the European regulatory standards [121]. Developing a cost-effective phage therapy module requires deliberation from both the legis­lative/regulatory bodies and the pharmaceutical industry. In Belarus, Russia, and Ukraine, a num­ber of companies including Microgen are already marketing phage cocktails for a number of infec­tions which are available as registered medicines [122]. Intralytics Inc. in the USA has developed a patented and FDA-approved phage cocktail against E. coli and Listeria monocytogenes for the food industry marketed as ListShield™ (http://intralytix.com/). It is hoped that coordi­nated efforts from the medical community, phar­maceutical companies, and legislative bodies will make phage therapy an economical and highly effective treatment option for the control of DRI.
9.8 Conclusions
Awareness regarding the potential of phage usage has increased manifold. Commercial patents afforded for biolm control of infections in food industry as well as the success of clinical trials worldwide are providing a major credence to phage therapy. It is hoped that combination treat­ments will gain popularity in mainstream medi­cine with phage treatment units in hospitals worldwide.
Acknowledgement Research grant from Chhatrapati Shahu Ji Maharaj University supports the work on bacte­riophage control that forms the basis of this manuscript.
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Extracellular Vesicles Derived
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fromMesenchymal Stem/Stromal Cells: Current Approaches toEnhance Their Release andTherapeutic Potential
RichardSchäfer, BenjaminKoch, andPatrickC.Baer
10
10.1 Introduction
Cell-based therapies have been widely used in experimental and clinical studies as a new thera­peutic approach for several diseases. In particu­lar, transplantation of mesenchymal stem/stromal cells (MSCs) is a very promising therapy option to support organ and tissue regeneration. During embryonic development MSCs originate from the somatic lateral plate mesoderm [1]. Later, MSCs can be isolated from umbilical cord/cord blood, amniotic uid and the placenta, but also from nearly all tissues and organs of the adult organism [2]. In vivo MSCs can be traced close to the vasculature, but they can also be detected in other distinct localizations such as the endos­teum or the medullary cavity of the bone [3, 4]. Observations that MSCs can be differentiated
R. Schäfer (*) Institute for Transfusion Medicine and Immunohematology, German Red Cross Blood Donor Service Baden-Württemberg-Hessen gGmbH, Goethe University Hospital, Frankfurt am Main, Germany e-mail: r.schaefer@blutspende.de
B. Koch · P. C. Baer Division of Nephrology, Department of Internal Medicine III, Goethe-University, Frankfurt am Main, Germany e-mail: B.Koch@med.uni-frankfurt.de
invitro into mesodermal lineages such as osteo­cytes, chondrocytes, and adipocytes [5] sug­gested a “stem cell” character of MSCs. However, this has been heavily debated due to lack of evi­dence, or at least inconsistent reproducibility, of functional MSCs’ transdifferentiation into non­mesodermal cell types [6]. Yet, the existence of MSCs subpopulations featuring different degrees of stemness or plasticity invivo and invitro can­not be completely ruled out [4, 6, 7].
Currently, the most widely used MSC isola­tion technique is outgrowth and subculturing of adherent broblastoid cells, and MSCs ex vivo expansion is feasible for up to 50 cumulative population doublings [8], hereby providing sub­stantial cell numbers for manufacture of MSC therapies. MSCs research has been growing steadily for decades, and MSCs productions for clinical applications are on the rise [9]. But what, besides their relatively simple isolation proce­dure and their exvivo upscaling potential, makes MSCs attractive as cell therapeutics for regenera­tive medicine? MSCs have been successfully evaluated for decades in a great variety of pre­clinical disease models such as cardiac and cere­bral ischemia, lung injury, bone defects, as well as autoimmune diseases [10–14]. Meanwhile, MSCs have been used in the clinic and current clinical indications for MSCs (mainly derived from bone marrow and adipose tissue) in regen­erative medicine, such as organ ischemia or
© Springer Nature Switzerland AG 2019 D. Duscher, M. A. Shiffman (eds.), Regenerative Medicine and Plastic Surgery,
https://doi.org/10.1007/978-3-030-19958-6_10
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