MEDICINAL PLANTS AND PHYTOCHEMICALS AGAINST PSEUDOMONAS AERUGINOSA QUORUM SENSING

MEDICINAL PLANTS AND PHYTOCHEMICALS AGAINST PSEUDOMONAS AERUGINOSA QUORUM SENSING

Jeevitha Murugesan and Shubashini K. Sripathi ^*

Department of Chemistry, Avinashilingam Institute for Home Science and Higher Education for Women Coimbatore - 641043, Tamil Nadu, India.

ABSTRACT: Medicinal plants are significantly used in the cure of various ailments from ancient times. Literature suggests that traditional medicinal plants from Fabaceae, Lamiaceae, Myrtaceae, and Anacardiaceae, Combretaceae family are widely studied, and they potentially inhibit quorum sensing, a bacterial communication mechanism that leads to the pathogenesis. Plants such as Anogeissus leiocarpus, Brassia oleraceae, Camellia nitidissima, Cassia alata, Laserpitium ochridanum, Neppenthes alata, Parkia javanica, Pistacia atlantica, Plantago asiatica, Psidium guajava, Quercus infectoria, Terminallia bellerica, Terminallia catappa, are reported to be effective in quorum sensing inhibition. Plant extracts containing phytochemicals such as quercetin, kaempferol, myricetin, baicalin, cassipourol, 6-gingerol and eugenol were reported to be potential inhibitors of Pseudomonas aeruginosa quorum sensing. Bioactive principles from medicinal plants with anti-quorum sensing properties are remarkable substitutes for synthetic antibacterial drugs, especially in the era of multi-drug resistant (MDR) pathogens. The anti-quorum sensing activity of medicinal plants against the Pseudomonas aeruginosa, a gram-negative MDR bacterium, is reviewed for the period from 1997 to 2019.

Medicinal plants, Quorum sensing, Quorum sensing inhibition, Pseudomonas aeruginosa

INTRODUCTION: Quorum sensing (QS) is a cell-to-cell communication process in bacteria to stimulate and respond based on population density through small signaling molecules ¹. Bacteria use QS systems to coordinate certain behaviors such as biofilm formation, virulence, and antibiotic production. Recently, quorum sensing has been shown to be involved in the development of resistance to various antimicrobial treatments and immune modulation.

A drug that is capable of blocking QS is likely to increase the susceptibility of the infecting organism to host defenses and its clearance from the host. Since pathogenicity in many bacteria is regulated by QS, inhibition of this mechanism may lead to the suppression of virulence ².

The use of quorum sensing inhibitors (QSI) to attenuate bacterial pathogenicity, is highly attractive, particularly with respect to the emergence of the multi-antibiotic resistant bacteria P. aeruginosa. Interference with quorum sensing could be a novel approach to control bacterial infections as many bacteria rely on quorum sensing ³. The World Health Organization (WHO) reported that 80% of the world’s population use herbal medicines for their primary healthcare ⁴. Natural products play a vital role in treating and preventing infectious diseases, and many approved drugs that we are using nowadays are derived from medicinal plants. To date, several studies have been focused on herbs that play a major role in the prevention, management, and treatment of various diseases due to their efficacy, less side effects, and relatively cost-effectiveness ⁵. Contribution of medicinal plants towards ayurvedic medicine increased the potentiality of plant-derived novel drugs that enhance human health via their medicinal properties ⁶. Here, we present an up-to-date review on medicinal plants with potential quorum sensing inhibitory effect with special emphasis on plant family, extraction methods, solvents used, and efficacy.

Multi-Drug Resistance: According to WHO, resistant microorganisms such as bacteria, fungi, viruses, and parasites can combat antimicrobial drugs, which leads to ineffective treatment resulting in the persistence of infections. Although the development of multidrug resistance is a natural phenomenon, its huge rise in recent years has become a major threat to mankind, especially among the immunocompromised individuals ⁷. The process of drug discovery of new antimicrobial drugs takes a long time.

Hence, only very few new agents have recently been approved by the FDA and are available for use. The Infectious Diseases Society of America (IDSA) recognizes anti-microbial resistance as “one of the greatest threats to human health worldwide” ⁸. Hence, the identification and evaluation of new antimicrobials with alternate strategy is much warranted.

Pseudomonas aeruginosa – A superbug: Pseudomonas aeruginosa is a life-threatening gram-negative bacterium in immunocompromised patients. It is a common cause of pneumonia, urinary tract and surgical-site infections, burn infections, and plays a vital role in cystic fibrosis infections. It can even lead to lethal conditions, especially due to its intrinsic resistance to antibiotics ⁹. It is one of the uropathogens that resist the action of several antibiotics due to biofilm formation ¹⁰. A range of mechanisms for adaptation, survival, and resistance against multiple classes of antibiotics makes P. aeruginosa the most emerging public health threat.

This bacterium is resistant to nearly against almost all antibiotics, including aminoglycosides, cephalo-sporins, fluoroquinolones and carbapenems ¹¹.

Quorum Sensing – A Promising Target: Quorum sensing is a promising target for the development of new anti-infectives ¹². Bacterial pathogens rely heavily on QS systems to control the expression of genes vital for virulence. Bacterial quorum sensing is regulated via small signaling molecules called autoinducers (AIs). In Gram-negative bacteria, QS systems are mainly based on LuxI/LuxR homo-logues. The LuxI homologs encode an AHL synthase involved in the synthesis of signal molecules, and the LuxR homologs encode the transcription regulatory protein, which, upon binding of the cognate signal molecules, activates the transcription to the QS target genes ¹³. At low cell density, the concentration of AHL is low, and unliganded LuxR receptors are intrinsically unstable and rapidly degradable. As cell density increases, the AHL concentration equally increases, and the accumulated AHLs interact with LuxR receptor, leading to stabilization of the protein-ligand complex. The LuxR: AHL complex binds DNA at promoters activating the genes under the control of quorum sensing ¹⁴. Many gram-negative organisms, including Pseudomonas aeruginosa, use AHL-type QS signals.

Quorum Sensing in P. aeruginosa: Pseudomonas spp., specifically P. aeruginosa, uses a complex network of quorum sensing receptors and AIs. The major P. aeruginosa receptors are LuxR-type receptors that, following autoinducer binding in the cytoplasm and function as DNA-binding trans-criptional activators. There are currently four well-known quorum sensing pathways in P. aeruginosa: two LuxR and LuxI-type systems called LasI/R and RhlI/R/the PqsR-controlled quinolone system and the IQS system that functions under phosphate-limiting conditions. However, the bacterium uses predominantly use LasI/LasR and RhlI/RhlR systems as two main pathways for quorum sensing ^{13, 15}. The systems are organized in a hierarchy with LasR at the top of the cascade. LasR, in complex with 3- oxo-C₁₂-HSL and activates a large regulon of downstream genes that includes the LasI synthase gene, which leads to the production of 3-oxo-C₁₂-HSL.

The LasR–3-oxo-C₁₂-HSL complex also activates the expression of RhlR and RhlI, which encode the second quorum sensing system ¹⁵ and the PqsR and PqsABCDH genes, which encode the PQS system. RhlR operates similarly to LasR and, when bound to C₄-HSL, activates its own regulon that includes RhlI and thereby establishes the second auto-induction feed-forward loop. Thus, it is revealed that the quorum sensing mechanism is directly or indirectly regulating the biofilm and virulence trait, in turn, executing the pathogenesis.

Inhibition of Quorum Sensing: Quorum sensing inhibitors (QSIs) are the molecules responsible for inhibition of quorum sensing systems, which leads to suppression of biofilm and virulence factors. It includes furanones and their related structural analogs ¹⁶, heavy metals ¹⁷ bismuth porphyrin complexes ¹⁸, glycosylated flavonoids ¹⁹, glycol-monoterpenols ²⁰ and nanomaterials ²¹. QS inhi-bitory activity is due to the structural similarity of furanones with AHLs, but some studies also showed that furanones might function through degrading of the LuxR-type protein ²² or lowering the DNA-binding activity of LuxR, the trans-criptional regulator protein ²³. Biofilm formation and QS-controlled virulence factors was reduced by furvina, sulphoraphane, and erucin ^{24, 25}.

Anti-quorum Sensing in Medicinal Plant Formulations: In Indian traditional medicine a formulation called Panchvalkal extract (Pentaphyte P5-capsule form) prepared with mixtures of bark extracts of Ficus racemosa, Albizzia lebbec, Ficus bengalensis, Ficus lacor and Ficus religiosa exerts anti-virulence effects by disrupting the QS mechanism ²⁶. Ethanol extract of traditional Thai herbal formulation “Ya-Samarn-Phlae” containing equal proportions of Oryza sativa L. (seed), Curcuma longa L. (rhizome), Areca catechu L. (seed) and Garcinia mangostana L. (pericarp) shows significant anti- Pseudomonas biofilm activity ²⁷. Notably, flavonoids and certain terpenoids containing plant extracts were found to show remarkable quorum sensing inhibition against P. aeruginosa. Aqueous extract of the Chinese medicine Yunnan Baiyao showed inhibitory activity against the virulence of P. aeruginosa ²⁸.

Medicinal Plant Extracts against Quorum Sensing: Various plants have been identified with the potential to disrupt bacterial quorum sensing (QS), which plays a key role in the regulation of virulence in many gram-positive and gram-negative bacteria ²⁹. Pyocyanin was remarkably reduced by Aegle marmelos. Enhanced cell adhesion inhibition was shown by Cynodon dactylon ³⁰. Rosina Khan has been reported that ethanol fraction of root of Zingiber officianalis showed high antiquorum activity ³¹. Ethanol extracts of leaves of Mangifera indica, Cassia alata, plant parts of Centilla asiatica, inhibited QS regulated phenotypes, a significant reduction in swarming ^{32, 33}.

Ethyl acetate fraction of Parkia javanica fruit extract (PJE) and Onion peel (ONE) inhibited the QS-mediated biofilm formation, EPS (Extracellular polymeric substances) production and swarming motility, elastase, pyocyanin production ^{34, 35}. Chloroform and petroleum extract of O. hadiense ³⁶ and the extract of T. bellerica has reduced the production of pyocyanin, exopolysaccharide, and biofilm formation in P. aeruginosa strains ³⁷. Dichloromethane extract of fig leaf inhibited QS regulated phenotypes ³⁸.

Gallic acid, catechin, ellagic acid, chlorogenic acid, quercetin, and kaempferol were identified in the Dichloromethane fraction of Camellia nitidissima flowers ³⁹. The aqueous leaf extract of Psidium guajava (GLE), Centella asiatica inhibits swarming motility of Pseudomonas aeruginosa ^{40, 32}. Reverse phase-solid phase extraction of aqueous leaf extract of Cassia alata inhibited biofilm formation of Pseudomonas aeruginosa ⁴¹. Plants from 61 distinct families were assessed for quorum sensing especially plants belonging to the families Fabaceae, Lamiaceae, Combretaceae, Myrtaceae, Zingiberaceae are widely studied, and they potentially inhibit quorum sensing Table 1.

Phytochemicals as Quorum Sensing Inhibitors: Major flavonoids, namely, quercetin, quercetrin, kaempferol, myricitin ^{42, 43}, flavanones like naringenin, eriodictyol and taxifolin ⁴⁴, baicalin ^{45, 34}, eugenol ⁴⁶, cassipoural ⁴⁷, flavonoids ⁴⁸ shows quorum sensing inhibitory activity. Coumarin, a natural plant phenolic compound, Cinnamon ^{49, 50}, Oleanolic aldehyde coumarate (OALC), a novel bioactive compound obtained from extracts of Dalbergia trichocarpa bark ⁵¹, 6-gingerol, a pungent oil of fresh ginger and Rosmarinic acid shows inhibition against Pseudomonas aeruginosa ^{52, 53}. Virulence factor production was suppressed by administration of flavonoids to P. aeroginosa. Especially structure activity relationship reveals that to inhibit LasR / RhlR, two hydroxyl moieties present in the flavone-A ring backbone is important ⁵⁴. Extracts of cauliflower, celery salt, chervil, garden cress, lemongrass, radish, thyme, water cress shows positive result QSI screening ⁵⁵. Mortality of C. elegans was inhibited by aqueous extracts of Conocarpus erectus, Callistemon viminalis, Bucida buceras ⁵⁶. Essential oils of cinnamon, lavender, and peppermint showed anti-QS activity ³¹.

Table 1 lists various plant extracts tested for anti-quorum sensing efficacy. Natural products from plant sources specifically tested for anti-quorum sensing efficacy against P. aeruginosa are listed in Table 2.

TABLE 1: MEDICINAL PLANTS AGAINST PSEUDOMONAS AERUGINOSA

TABLE 2: NATURAL PRODUCTS FROM PLANT SOURCES SPECIFICALLY TESTED FOR ANTI-QUORUM SENSING EFFICACY AGAINST P. AERUGINOSA

FIG. 1: COMPARISON OF ANTI-QUORUM SENSING ACTIVITY OF VARIOUS PLANT FAMILIES AGAINST PSEUDOMONAS AERUGINOSA

FIG 2: PERCENTAGE OF PLANT PARTS USED IN ANTI-QUORUM SENSING STUDIES AGAINST PSEUDOMONAS AERUGINOSA

CHART 3: STRUCTURE OF PHYTOCHEMICALS TESTED AGAINST PSEUDOMONAS AERUGINOSA

FIG. 4: VARIOUS SOLVENTS USED FOR PLANT EXTRACTION FOR ANTI-QUORUM STUDIES AGAINST PSEUDOMONAS AERUGINOSA

FIG. 5: DIFFERENT EXTRACTION METHODS USED FOR ANTI-QUORUM STUDIES AGAINST PSEUDOMONAS AERUGINOSA

Fig. 1 shows the comparison of anti-quorum sensing activity of various plant families against Pseudomonas aeruginosa. Fig. 2 gives details of various plant parts used for anti-quorum sensing. Chart 3 represents the structures of phytochemical compounds tested against P. aeruginosa. Though various solvents are used for plant extraction for anti-quorum studies against Pseudomonas aeruginosa polar solvents are mostly used, and the polar extracts show good inhibitory activity Fig. 4. Plant materials tested for quorum sensing have been extracted by soaking and soxhlet extraction methods predominantly Fig. 5.

FIG. 6: PROGRESS ON ANTI-QUORUM STUDIES AGAINST PSEUDOMONAS AERUGINOSA

In the last one decade the number of reports on quorum sensing with medicinal plants has increased Fig. 6.

CONCLUSION: Traditional medicinal plants have been proved for their potential anti-quorum sensing activities against Pseudomonas aeruginosa. Polar extracts of plants are found to have significant activity when compared to other solvents.

Various types of phytochemicals extracted from these medicinal plants, especially flavonoids compounds are proved to be effective in down regulating quorum sensing in Pseudomonas aeruginosa. Plant extracts showing potential anti-quorum sensing activity with low MIC values are Psidium guajava, Cassia alata, Camellia nitidissima, Anogeissus leiocarpus, Parkia javanica, Terminallia catappa, Neppenthes alata, Brassia oleraceae, Plantago asiatica, Terminallia bellerica, Quercus infectoria, Pistacia atlantica and Laserpitium ochridanum. Since many of the modern-day medicines are of plant origin, these plant extracts may be further explored to develop as a potential alternative to reduce the misuse and overuse of antibiotics on human and animal health.

From among the tested compounds cinnamon oil showed the lowest MIC value (0.0001 mg/ml) followed by norfloxacin (0.00025 mg/ml), chrysin (0.025 mg/ml) and curcumin (0.030 mg/ml). Phytochemistry, through the simultaneous use of inhibitors for different targets / QS schemes, could also be of tremendous benefit in the fight against multiantibiotic bacterial diseases.

FUTURE PERSPECTIVES: With the remarkable technical advances in medicinal chemistry, molecular entities, especially of plant origin, which have not been investigated till date can be analyzed for anti-quorum sensing activity. Based on the potency of such compounds and their derivatives, future assessment can be performed through pre-clinical and clinical trials. In order to mitigate misuse and overuse of antibiotics on human health and the environment, this active area will require a great deal of focus. It is important to note, that QS inhibitors especially from plant sources are most likely to be beneficial when co-administered with conventional antibiotics as adjuvants rather than as standalone therapeutic agents.

ACKNOWLEDGEMENT: The authors thank Avinashilingam Institute for Home Science and Higher Education for Women for support and facilities. One of the authors M. Jeevitha, acknowledges funding received from the Department of Science and Technology under the WOS-A scheme for the study (SR/WOS-A/CS-25/2018).

CONFLICTS OF INTEREST: Nil

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     How to cite this article:

     Murugesan J and Sripathi SK: Medicinal plants and phytochemicals against Pseudomonas aeruginosa quorum sensing. Int J Pharm Sci & Res 2020; 11(10): 4749-73. doi: 10.13040/IJPSR.0975-8232.11(10).4749-73.

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