Sains Malaysiana 52(1)(2023):
199-210
http://doi.org/10.17576/jsm-2023-5201-16
In Vitro Antimicrobial,
Antiglycolytic, and Antibiofilm Activities of Synthetic 1,4-Naphthoquinone
Derivatives against Cariogenic Bacteria
(Aktiviti Antimikrob, Antiglikolitik dan Antibiofilem In Vitro bagi Terbitan 1,4-Naftokuinon
Sintetik terhadap Bakteria Kariogenik)
PICHAYAPORN
RATTI1, JUTHARAT MANUSCHAI1, JIRAPORN KARA2,3,
LUELAK LOMLIM2,3 & SUPAWADEE NAORUNGROJ1,*
1Department of
Conservative Dentistry, Faculty of Dentistry, Prince of Songkla University, Hat Yai, Songkhla, Thailand
2Department of
Pharmaceutical Chemistry, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Hat Yai,
Songkhla, Thailand
3Phytomedicine and
Pharmaceutical Biotechnology Excellent Center (PPBEC), Faculty of
Pharmaceutical Sciences, Prince of Songkla University, Hat Yai, Songkhla, Thailand
Diserahkan:
11 Jun 2022/Diterima: 29 September 2022
Abstract
This study investigated the
potential anticaries properties of synthetic
1,4-naphthoquinone derivatives. Synthetic 1,4-naphthoquinone
derivatives (2-4) were designed and synthesized by employing lawsone methyl ether (LME, 1), a plant-derived
1,4-naphthoquinone, as a lead compound. The synthetic compounds were
characterized by infrared spectroscopy, 1H-nuclear magnetic
spectroscopy, 13C- nuclear magnetic spectroscopy, and
high-resolution mass spectrometry. Minimum inhibitory concentration (MIC),
minimum bactericidal concentration (MBC), and growth curves were determined to
assess their antibacterial effects against Streptococcus mutans, Lacticaseibacillus casei,
and Actinomyces naeslundii. The pH drop assay
was also performed on these three bacterial species. The effect on S. mutans biofilm formation was evaluated by crystal
violet assay. From the microdilution assay, 2-(prop-2-ynyloxy) naphthalene-1,4-dione
(compound 2) showed potent antimicrobial activity against S. mutansand A. naeslundii(MIC
of 1.56 and 3.125 µg/mL, respectively) in the same range as chlorhexidine (MIC
of 1.95 and 1.95 µg/mL, respectively). The 1,4-naphthoquinone derivatives
showed low antibacterial activity against L. casei.
LME (compound 1) and 2-(prop-2-ynyloxy) naphthalene-1,4-dione
(compound 2) inhibited pH reduction from S. mutans.
The compounds at sub-MIC concentrations showed a potent inhibitory effect
against S. mutans biofilm formation in a dose-
and time-dependent manner. These results suggested that the synthetic
1,4-naphthoquinone derivatives are promising compounds that could be developed
as a novel alternative or adjunctive anticaries therapies.
Keywords: Acid production; antibacterial activity;
dental biofilm; dental caries; 1,4-naphthoquinone
Abstrak
Penyelidikan ini mengkaji potensi
sifat antikaries bagi terbitan 1,4-naftokuinon sintetik. Terbitan
1,4-naftokuinon sintetik (2-4) telah
direka dan disintesis dengan menggunakan lawsone metil eter (LME, 1), 1,4-naftokuinon yang berasal
daripada tumbuhan, sebagai sebatian plumbum. Sebatian sintetik telah dicirikan oleh spektroskopi
inframerah, spektroskopi magnet nuklear 1H, spektroskopi magnet
nuklear 13C dan spektrometri jisim resolusi tinggi. Kepekatan
perencatan minimum (MIC), kepekatan bakteria minimum (MBC) dan lengkung
pertumbuhan ditentukan untuk menilai kesan antibakteria mereka terhadap Streptococcus mutans, Lacticaseibacillus
casei dan Actinomyces naeslundii. Ujian
penurunan pH juga dilakukan ke atas ketiga-tiga spesies bakteria ini. Kesan ke atas
pembentukan biofilem S. mutans dinilai
dengan ujian kristal violet. Daripada ujian pencairan mikro,
2-(prop-2-yniloksi)naftalena-1,4-dion (sebatian 2) menunjukkan aktiviti antimikrob yang kuat terhadap S. mutans dan A. naeslundii (masing-masing MIC 1.56 dan 3.125 µg/mL) dalam julat yang
sama seperti klorheksidin (masing-masing MIC 1.95 dan 1.95 µg/mL). Terbitan
1,4-naftokuinon menunjukkan aktiviti antibakteria yang rendah terhadap L. casei. LME (sebatian 1) dan
2-(prop-2-yniloksi)naftalena-1,4-dione (sebatian 2) menghalang pengurangan pH daripada S. mutans. Sebatian pada kepekatan sub-MIC menunjukkan kesan
perencatan yang kuat terhadap pembentukan biofilem S. mutans dalam cara yang bergantung kepada dos dan masa. Keputusan ini
mencadangkan bahawa terbitan 1,4-naftokuinon sintetik adalah sebatian yang
menyakinkan dan boleh dibangunkan sebagai alternatif baru atau terapi
antikaries tambahan.
Kata kunci: Aktiviti antibakteria; biofilem gigi; karies gigi; penghasilan asid; 1,4-naftokuinon
RUJUKAN
Ahn, S.J., Wen, Z.T. & Burne,
R.A. 2007. Effects of oxygen on virulence traits of Streptococcus mutans. Journal of Bacteriology 189(23): 8519-8527.
Alaki,
S.M., Burt, B.A. & Garetz, S.L. 2009. The association between antibiotics
usage in early childhood and early childhood caries. Pediatric Dentistry 31(1): 31-37.
Anaissi-Afonso,
L., Oramas-Royo, S., Ayra-Plasencia, J., Martín-Rodríguez, P., García-Luis, J.,
Lorenzo-Castrillejo, I., Fernández-Pérez, L., Estévez-Braun, A. & Machín,
F. 2018. Lawsone, Juglone, and β-Lapachone derivatives with enhanced
mitochondrial-based toxicity. ACS Chemical Biology 13(8): 1950-1957.
Azeredo,
J., Azevedo, N.F., Briandet, R., Cerca, N., Coenye, T., Costa, A.R., Desvaux,
M., di Bonaventura, G., Hébraud, M., Jaglic, Z., Kačániova, M., Knøchel, S., Lourenço, A., Mergulhão,
F., Meyer, R.L., Nychas, G., Simões, M., Tresse, O. & Stenberg, C. 2017.
Critical review on biofilm methods. Critical Reviews in Microbiology 43(3): 313-351.
Caufield,
P.W., Schön, C.N., Saraithong, P., Li, Y. & Argimón, S. 2015. Oral
lactobacilli and dental caries: A model for niche adaptation in humans. Journal
of Dental Research 94(9 Suppl): 110S-8S.
Dieterle,
M.E., Fina Martin, J., Durán, R., Nemirovsky, S.I., Sanchez Rivas, C., Bowman,
C., Russell, D., Hatfull, G.F., Cambillau, C. & Piuri, M. 2016.
Characterization of prophages containing "evolved" Dit/Tal modules in
the genome of Lactobacillus casei BL23. Applied Microbiology and
Biotechnology 100(21): 9201-9215.
Han,
S., Abiko, Y., Washio, J., Luo, Y., Zhang, L. & Takahashi, N. 2021. Green
tea-derived epigallocatechin gallate inhibits acid production and promotes the
aggregation of Streptococcus mutans and non-mutans streptococci. Caries Research 55(3): 205-214.
Howell,
A., Jordan, H.V., Georg, L.K. & Pine, L. 1965. Odontomyces viscosus, gen. nov., spec. nov., a filamentous
microorganism isolated from periodontal plaque in hamsters. Sabouraudia 4(2): 65-68.
Jeon,
J.G., Rosalen, P.L., Falsetta, M.L. & Koo, H. 2011. Natural products in
caries research: Current (limited) knowledge, challenges and future
perspective. Caries Research 45(3): 243-263.
Kawashima,
J., Nakajo, K., Washio, J., Mayanagi, G., Shimauchi, H. & Takahashi, N.
2013. Fluoride-sensitivity of growth and acid production of oral Actinomyces:
Comparison with oral Streptococcus. Microbiology and Immunology 57(12): 797-804.
Levison,
M.E. 2004. Pharmacodynamics of antimicrobial drugs. Infectious Disease
Clinics of North America 18(3): 451-465.
Li, J.,
Helmerhorst, E.J., Leone, C.W., Troxler, R.F., Yaskell, T., Haffajee, A.D.,
Socransky, S.S., & Oppenheim, F.G. 2004. Identification of early microbial
colonizers in human dental biofilm. Journal of Applied Microbiology 97(6): 1311-1318.
Lopez,
L.I.L., Flores, S.D.N., Belmares, S.Y.S. & Galindo, A.S. 2014.
Naphthoquinones: Biological properties and synthesis of lawsone and derivatives
- A structured review. Vitae 21(3): 248-258.
Nittayananta,
W., Limsuwan, S., Srichana, T., Sae-Wong, C. & Amnuaikit, T. 2018. Oral
spray containing plant-derived compounds is effective against common oral
pathogens. Archives of Oral Biology 90: 80-85.
Panichayupakaranant,
P. & Reanmongkol, W. 2008. Evaluation of chemical stability and skin
irritation of lawsone methyl ether in oral base. Pharmaceutical Biology 40(6): 429-432.
Panichayupakaranant,
P., Septama, A.W. & Sinviratpong, A. 2019. Synergistic activity of lawsone
methyl ether in combination with some antibiotics and artocarpin against
methicillin-resistant Staphylococcus aureus, Candida albicans,
and Trychophyton rubrum. Chinese
Herbal Medicines 11(3): 321-325.
Qiu,
W., Zhou, Y., Li, Z., Huang, T., Xiao, Y., Cheng, L., Peng, X., Zhang, L. &
Ren, B. 2020. Application of antibiotics/antimicrobial agents on dental caries. Biomed Research International 2020: 5658212.
Sakunphueak,
A. & Panichayupakaranant, P. 2012. Comparison of antimicrobial activities
of naphthoquinones from Impatiens
balsamina. Natural Product Research 26(12): 1119-1124.
Simón-Soro,
A. & Mira, A. 2015. Solving the etiology of dental caries. Trends in
Microbiology 23(2): 76-82.
Taff,
H.T., Nett, J.E. & Andes, D.R. 2012. Comparative analysis of candida
biofilm quantitation assays. Medical Mycology 50(2): 214-218.
Takahashi,
N. & Nyvad, B. 2016. Ecological hypothesis of dentin and root Caries. Caries
Research 50(4): 422-431.
Tanner,
A., Kressirer, C.A., Rothmiller, S., Johansson, I. & Chalmers, N.I. 2018.
The caries microbiome: Implications for reversing dysbiosis. Advances in
Dental Research 29(1): 78-85.
ten
Cate, J.M. & Zaura, E. 2012. The numerous microbial species in oral
biofilms: How could antibacterial therapy be effective? Advances in Dental
Research 24(2): 108-111.
van der
Hoeven, J.S. & van den Kieboom, C.W.A. 1990. Oxygen-dependent lactate
utilization by Actinomyces viscosus and Actinomyces naeslundii. Oral Microbiology and Immunology 5(4):
223-225.
Vohra,
F., Akram, Z., Safii, S.H., Vaithilingam, R.D., Ghanem, A., Sergis, K. &
Javed, F. 2016. Role of antimicrobial photodynamic therapy in the treatment of
aggressive periodontitis: A systematic review. Photodiagnosis and
Photodynamic Therapy 13: 139-147.
Wilkins,
J.C., Homer, K.A. & Beighton, D. 2002. Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Applied and
Environmental Microbiology 68(5): 2382-2390.
Yang,
X., Summerhurst, D.K., Koval, S.F., Ficker, C., Smith, M.L. & Bernards,
M.A. 2001. Isolation of an antimicrobial compound from Impatiens balsamina L. using bioassay-guided fractionation. Phytotherapy
Research 15(8): 676-680.
Zotta,
T., Parente, E. & Ricciardi, A. 2017. Aerobic metabolism in the genus
Lactobacillus: Impact on stress response and potential applications in the food
industry. Journal of Applied Microbiology 122(4): 857-869.
*Pengarang untuk surat-menyurat; email: supawadee.n@psu.ac.th
|