DBPIA-NURIMEDIA

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1 Korean Society for Biotechnology and Bioengineering Journal 30(5): (2015) ISSN / eissn 연구논문 한국여성의질에서분리한유산균의 Gardnerella vaginalis 에대한항균효과및특성규명 김용경 1, 강창호 1, 신유진 1, 백남수 2, 소재성 1 * Characterization and Antimicrobial Activity against Gardnerella vaginalis of Vaginal Lactobacillus spp. Isolated from Korean Women YongGyeong Kim 1, Chang-Ho Kang 1, YuJin Shin 1, Nam-Soo Paek 2, and Jae-Seong So 1 * Received: 21 July 2015 / Revised: 16 September 2015 / Accepted: 22 October The Korean Society for Biotechnology and Bioengineering Abstract: Bacterial vaginosis (BV) is caused by microbial imbalance of the vaginal ecosystem and overgrowth of anaerobic bacteria. The antibiotic treatment often results in very high recurrence of BV because it disturbs the vaginal ecosystem. The high recurrence rates suggest a need for alternative therapeutic methods and probiotics are being recognized as alternative or additional treatment method for BV. The purpose of this study was to investigate how human vaginal isolates of Lactobacillus spp. inhibit the BV-associated pathogen Gardnerella vaginalis. Results show that selected strains significantly reduced the viability of G. vaginalis. Among these selected strains KLB410 and KLB416 were further selected based on acid/bile tolerance and identified through 16S rrna gene sequencing being Lactobacillus plantarum. Further studies are underway to demonstrate that the selected strain can be applied as potential probiotics for recovering vaginal ecosystem. Key words: Bacterial vaginosis, Gardnerella vaginalis, Probiotics, Lactobacillus spp. 1 인하대학교생물공학과 1 Department of Biological Engineering, Inha University, Incheon 22212, Korea Tel: , Fax: sjaeseon@inha.ac.kr 2 ( 주 ) 메디오젠 2 MEDIOGEN, Co., Ltd, Seoul , Korea 1. INTRODUCTION 세균성질증 (bacterial vaginosis) 이란질내의건강을유지하는유산균총이감소하여혐기성병원균인 Gardnerella vaginalis, Mycoplasma hominis, Prevotella spp. 등이질내에서증식하면서발생하게되는질병이다 [1]. 질내에서혐기성병원균이증식하게되면질내휘발성아민화합물이증가하며, 이는세균성질증특유의악취를유발하게된다 [2]. 또한산성으로유지되는질내산도가높아져임신관련질병및성병감염의위험을높인다고알려져있다 [3,4]. 이러한세균성질증의치료는주로 metronidazole, clindamycin 등의항생제를복용또는주입하는방법이사용되고있지만, 지속적으로재발하는문제점이있다 [5]. 따라서기존의항생제사용의보완방안으로병원균의제거뿐만아니라질내환경을개선하여세균성질증이재발하는것을방지하는방안등이연구되고있으며, 그대안방안으로살아있는생균제인프로바이오틱스를사용하는방법이주목을받고있다 [6]. 건강한여성의질에는다양한유산균들이존재하는데, 이러한유산균들은젖산을생성하고아민화합물을분해하여질내산도를낮추며, 과산화수소, 박테리오신등의항균물질을생산하여병원균감염을막고질내환경을건강하게유지시킨다 [7]. 선진국을중심으로요거트, 유산균캡슐을섭취하거나탐폰, 질정의형태로유산균을질내주입하는등, 질내환경개선을도와주는다양한형태의프로바이오틱스에대한연구 [8] 가진행되고있다. 하지만국내에서는유산균을통한질내환경개선에대한연구가매우미비한수준이다.

2 240 Korean Society for Biotechnology and Bioengineering Journal 30(5): (2015) 따라서본연구는세균성질증의치료및재발방지를위한대체방안의일환으로한국여성의질에서분리한유산균의프로바이오틱스로의가능성을확인하고, 세균성질증의주요원인균인 Gardnerella vaginalis 에대한항균효과를확인하였다. 또한항균활성이우수한유산균주를선별하여산성과담즙염에대한내성및 autoaggregation 특성을확인하여프로바이오틱스로서의기능확인을통해관련연구의기초자료로사용하고자한다. 2. MATERIALS AND METHODS 2.1. Gardnerella vaginalis 에대한항균효과본연구에서는한국여성의질에서분리한유산균 90 여종 [9] 을사용하였으며, 액체배지희석법을이용해세균성질증의주요원인균인 Gardnerella vaginalis KCTC5096 (G. vaginalis) 에대한항균력을확인하였다. 유산균주의배양은 MRS 배지 (Difco, MI, USA) 를사용하였으며, MRS 액체배지에 24 시간정치배양한배양액을 OD (10 8 ~10 9 CFU/mL) 으로조정하여새로운 MRS 배지에 1% 접종하였다. 18 시간동안배양한후, 원심분리 (4,000 g, 4 o C, 5 분 ) 하여 0.22 µm 필터를이용하여상등액을여과하여본실험에사용하였다. G. vaginalis 의배양은 10% 말혈청 (Horse serum, Life technologies corp., NY, USA) 을함유한 BHI 배지 (Difco, MI, USA) 를사용하였으며, Anaerocult A (Merck, Germany) 로혐기상태로 37 o C 에서 24 시간정치배양하였다. G. vaginalis 에대한항균효과는각각의유산균주의상등액을 10% 말혈청이포함된 5 ml BHI 배지에 10% 첨가한후, G. vaginalis 를 OD 로조정하여 1% 접종하였다. 24 시간동안혐기배양한뒤 G. vaginalis 의생균수를아래와같이측정하여분리균주의 G. vaginalis 에대한항균효과를확인하였다. 항균효과 (%) = [ 대조군 (CFU/mL) 실험군 (CFU/mL)] / 대조군 (CFU/mL) 선별된유산균주의산성및담즙염내성확인섭취하는유산균이질증개선에효과가있었다는연구 [8] 에기초하여, G. vaginalis 에대한항균효과가높은유산균주를선별한뒤장내환경과같은산성및담즙염에대한생균력을확인하기위해 Guo 의방법 [10] 으로실험을진행하였다. 선별된유산균주를 MRS 배지에 24 시간전배양한뒤, OD 으로조정하여새로운 MRS 배지에 1% 접종하여 18 시간배양하였다. 배양액은원심분리 (4,000 g, 4 o C, 5 분 ) 한후, phosphate-buffer saline (PBS, ph 7) 에 2 번세척하였고, OD ( CFU/mL) 으로조정하여각각산성과담즙염에대한내성실험에사용하였다. 산성에대한내성을확인하기위하여유산균희석액 1 ml 를 9 ml PBS (ph 2 와 7) 에첨가후진탕한뒤 37 o C 에서 3 시간배양한후생균수를확인하였다. 최종선별된유산균은 ph 2 에서 7 까지산성에대한내성 을확인하였다. 담즙염내성은 1% oxgall (Difco, MI, USA) 을포함한 MRS 배지에유산균희석액을 1% 접종하고 37 o C 에 24 시간배양한후생균수를확인하였다 Autoaggregation G. vaginalis 에대한항균효과가우수한유산균주를선별하여장내세포내부착능력을간접적으로확인하기위하여 Kassa 의연구 [11] 를변형하여 autoaggregation 실험을진행하였다. MRS 배지에유산균을전배양한배양액을 OD 으로조정하여새로운 5 ml MRS 배지에 1% 접종한뒤, 18 시간배양하여실험에사용하였다. 배양한유산균은원심분리 (4,000 g, 4 o C, 5 분 ) 한후, PBS 에 2 번세척하였고, OD ( CFU/mL) 으로조정하여균주현탁액 5 ml 을 10 초간진탕한뒤 5 시간동안방치하면서 autoaggregation 을확인하였다. 실험시작직후 (A0) 와 5 시간후 (A), 각각 0.1 ml 의상등액을취해 0.9 ml PBS 와혼합한뒤 600 nm 에서흡광도를측정 (A0, A) 하였고, 다음계산식에따라 autoaggregation 을계산하였다. Autoaggregation (%) ( A0 A) = A0 3. RESULTS AND DISCUSSION 3.1. Gardnerella vaginalis 에대한항균효과세균성질증을일으키는주요원인균중 G. vaginalis 는통성혐기성세균으로질내에서증식하면서질내산도를 ph 4.5 이상으로높이고, 이로인해다른병원성세균이증식할수있는환경을만들면서세균성질증을일으킨다고알려져있다 [12]. 최근에는 G. vaginalis 는 biofilm 부착력이뛰어나고부착후다른세균성질증균들의부착을증진시킨다고보고되고있다 [13]. 따라서본연구에서는국내여성의질에서분리한유산균주를질증의주요원인균인 G. vaginalis 를대상으로항균력실험을진행하였다. 분리된유산균주 90 종에대한 G. vaginalis 의항균효과는평균 45.02% 였으며이중높은항균력을나타내는 9 균주 (KLB403, KLB404, KLB407, KLB 408, KLB409, KLB410, KLB411, KLB413, KLB416) 의항균효과는평균 99.27% 이었다 (Fig. 1). 유산균은배양과정중젖산, 과산화수소, 박테리오신등을생산하며, 이를통해항균효과를보이는것으로알려져있으며 [7], 1 차선별한 9 균주는이러한항균물질생산능이다른분리균주보다높은균주로사료되며앞으로정확한항균물질에대한연구가필요하다 선별균주의산성및담즙염에대한내성확인일반적으로프로바이오틱스에사용되는유산균은섭취시위와장을거치며생균력이낮아지게되므로낮은산도와담즙염에대한내성능력은유용미생물로사용하기위하여필

3 한국여성의질에서분리한유산균의 Gardnerella vaginalis 에대한항균효과및특성규명 241 Fig. 1. Inhibition effect of cell free supernatants of vaginal lactobacilli antagonistic to Gardnerella vaginalis. 수적으로지녀야하는요소이다 [14]. 따라서본연구에서는 G. vaginalis 에대해높은항균효과를보인 9 균주에대해서산성및담즙염에대한내성을확인하였다 (Table 1). 산성에대한내성실험의결과, ph 2 에서 KLB413 (4.73 log CFU/mL) 과 KLB416 (4.66 log CFU/mL) 균주를제외한 7 균주에서는 10 4 CFU/mL 이하의생균수를보이는것을확인할수있었다. 또한 ph 7 에서의생균수대비 ph 2 에서의생균수가가장높은균주는 KLB416 으로 0.17% 의생존률을나타내었다. KLB416 은 ph 7 에서 ph 4 까지생균수에변화가없지만, ph 가낮아질수록생균수가감소하는것을확인할수있 었다 (Fig. 2). Guo [10] 와 Tasi [15] 의연구에서도본연구와유사한결과를확인할수있었다. 체내위액의 ph 는대략 3.0 으로유지되며, 일반적으로 ph 3 에서 3 시간이상생균수를유지하면산성에높은내성을보이는것으로알려져있다 [10]. Mishra 의연구 [16] 에서프로바이오틱스로사용되는여러균주들의산성에대한내성을살펴보면, ph 2 에서모든균주가 10 4 CFU/mL 이하의생균수를보이는것을확인할수있는데, 본연구에사용된 KLB416 균주의경우 ph 3 에서 6.47 log CFU/mL, ph 2 에서 4.66 log CFU/mL 의생균수를유지하여산성에대해우수한내성능력을가지고있는것을

4 242 Korean Society for Biotechnology and Bioengineering Journal 30(5): (2015) Table 1. Effect of ph and bile salt on the survival of selected strains Selected strains ph tolerance 1) Bile-salts tolerance 2) ph 7 ph2 0% 1% KLB ± 0.04 <2 3) 9.63 ± ± 0.03 KLB ± ± ± ± 0.00 KLB ± ± ± ± 0.05 KLB ± ± ± ± 0.06 KLB ± ± ± ± 0.04 KLB ± ± ± ± 0.30 KLB ± ± ± ± 0.19 KLB ± ± ± ± ) The ph tolerance results are shown the viable counts (log CFU/mL) of each isolate at ph 7 and ph 2 for 3 h. 2) Bile-salts tolerance results are shown as the viable counts (log CFU/mL) of each isolate at MRS media with 0 % and 1 % Oxgall at 37 o C for 24 h. 3) Below 2.00 log CFU/mL. Fig. 2. Survivability of KLB416 in acid condition for 3 h. Fig. 3. The autoaggregation ability for 5 h. 확인할수있다. 프로바이오틱스에사용되는유산균이위에서견디기위해산성내성을지녀야한다면장내극한환경에서생존하기위해서는쓸개에서분비되는담즙에대한내성을지녀야한다 [14]. 일반적으로유산균의담즙염에대한내성을확인하기위해서는일반적으로 0.3% 의담즙염이사용되고있는데 [17], Lin 의연구결과 [18] 에서 0.3% 담즙염에서유산균들의생균수가 10 4 CFU/mL 이하로담즙염에민감하다고알려져있다. 그러나본연구에서선별된 9 균주들은 1 % 담즙염농도에서도평균 8.03 log CFU/mL 의매우높은생균수를보여, 담즙염에대해매우우수한내성을보이는것을확인할수있다 Autoaggregation 프로바이오틱스로사용되는유산균의경우, 체내에서지속적으로작용하기위해서장및질세포에부착할수있는세포부착능이요구된다 [19]. Autoaggregation 능력은세포부착능을간접적으로확인할수있는방법으로, Del [19] 과 Kos [20] 의연구결과에따르면, autoaggregation 능력이높은균주가실제세포부착능력또한높다고알려져있다. 이에 G. vaginalis 에높은항균능력을보이는 9 균주를대상으로장내부착성을알아보기위하여 autoaggregation 실험을진행하였다 (Fig. 3). 선별된 9 균주에대한 autoaggregation 능력은평균 50.36% 였으며이중 KLB410 균주가 71.82% 로가장높은 autoaggregation 능력을나타내었다. Malik 의연구결과 [21] 에따르면, L. plantarum CMPG5300 의 in vitro 상의 autoaggregation 이약 70% 로나타났으며, in vivo 상인질상피세포에서의부착능도 50% 로 in vitro 상의결과와 in vivo 상의결과가연관되어진다고보고되었다. 세포부착능이뛰어난균주는세포에자리를잡아병원균의세포부착을막아감염을막는특성을가지는것으로알려져있으며 [7], 본연구에서선별된 KLB410 균주또한질내세포에높은부착능력을통해추가적인병원균감염을예방할수있을것이라사료된다 계통수분석본연구에서 G. vaginalis 에높은항균능력을보인 9 균주중, 산성환경에서내성이우수한 KLB416 균주와 autoaggregation 능력이우수한 KLB410 균주의 16S rrna gene sequencing 결과, Lactobacillus plantarum 으로동정되었다 (Fig. 4). L. plantarum KLB410 과 L. plantarum KLB416 균주는각각 National Center of Biotechnology Information 으로부터 accession number KM (KLB416), KT (KLB410) 을부여받았다. L. plantarum 은유제품, 고기, 발효된채소에다량함유되어있을뿐만아니라, 사람의체내에도상존하는균

5 한국여성의질에서분리한유산균의 Gardnerella vaginalis 에대한항균효과및특성규명 243 Fig. 4. Phylogenetic analysis of selected Lactobacillus spp. compared to other lactobacilli. 주로잘알려져있다 [22]. 또한 L. plantarum 는식품의약안전처건강기능식품의기준및규격 [23] 에등재되어안전성이확인된균주이다. 4. CONCLUSION 본연구는한국여성질에서분리한유산균을통해세균성질증의치료일환으로주요원인균인 Gardnerella vaginalis 에대해항균효과를확인하였다. 항균효과가높은 9 균주의 G. vaginalis 에대한평균항균효과는 99.27% 였으며, 항균효과가우수한균주를대상으로추가적인특성확인을위해산성및담즙염에대한내성과 autoaggregation 을확인하였다. 산성환경에서내성이가장우수한 KLB416 균주와 autoaggregation 능력이가장우수한 KLB410 균주는모두 Lactobacillus plantarum 으로동정되었으며, L. plantarum 은건강기능식품의기준및규격에등재되어있는균주로그안전성이이미입증되어있다. 이에최종선별된 L. plantarum KLB410 균주와 L. plantarum KLB416 균주는향후질건강을위한프로바이오틱스개발분야에주요한소재자원으로활용될수있을것이라기대된다. 추후선별된유산균주는프로바이오틱스로개발하기위하여위액과장액에서의안정성실험및동결건조보호제최적화연구를진행할것이다. REFERENCES 1. Mastromarino, P., B. Vitali, and L. Mosca (2013) Bacterial vaginosis: A review on clinical trials with probiotics. New Microbiologica 36: Chen, K. C., P. S. Forsyth, T. M. Buchanan, and K. K. Holmes (1979) Amine content of vaginal fluid from untreated and treated patients with nonspecific vaginitis. J. Clin. Invest. 63: Verstraelena, H., and A. C Senok (2005) Vaginal lactobacilli, probiotics, and IVF. Reprod. Biomed. Online 11: Wiesenfeld, H. C, S. L. Hillier, M. A. Krohn, D. V. Landers, and R. L. Sweet (2003) Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin. Infect. Dis. 36: Bradshaw, C. S., A. N. Morton, J. Hocking, S. M. Garland, M. B. Morris, L. M. Moss, L. B. Horvath, I. Kuzevska, and C. K. Fairley (2006) High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J. Infect. Dis. 193: Falagas, M. E., G. I. Betsi, and S. Athanasiou (2007) Probiotics for the treatment of women with bacterial vaginosis. Clin. Microbiol. Infect. 13: Borge, S., J. Silva, and P. Teixeira (2013) The role of lactobacilli and probiotics in maintaining vaginal health. Arch. Gynecol. Obstet. 289: Bastani, P., A. Homayouni, S. Ziyadi, and V. G. Tabrizian (2012) Dairy Probiotic Foods and Bacterial Vaginosis: A Review on Me-

6 244 Korean Society for Biotechnology and Bioengineering Journal 30(5): (2015) chanism of Action. pp In: Probiotics, Rigobelo, E. C. (Ed.), Intech., USA. 9. Chang, C. E., S. I. Pavlova, L. Tao, E. Kim, S. C. Kim, H. S. Yun and J. S. So (2002) Molecular Identification of Vaginal Lactobacillus spp. Isolated from Korean Women. J. Microbiol. Biotechnol. 12: Guo, X. H., J. M. Kim, H. M. Nam, S. Y. Park and J. M. Kim (2010) Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe 16: Kassa, I. A., M. Hamze, D. Hober, N. E. Chihib and D. Drider (2014) Identification of Vaginal Lactobacilli with Potential Probiotic Propertied Isolated from Women in North Lebanon. Microb. Ecol. 67: Borchardt, K. A., B. S. Adly, R. F. Smith, J. Eapen, and C. B. Beal (1989) Importance of Gardnerella vaginalis as an aetiological agent in bacterial vaginosis. Genitourin. Med. 65: Machado, A., K. K. Jefferson, and N. Cerca (2013) Interactions between Lactobacillus crispatus and Bacterial Vaginosis (BV)-associated bacterial species in initial attachment and biofilm formation. Int. J. Mol. Sci. 14: Dunne, C., L. O Mahony, L. Murphy, G. Thornton, D. Morrissey, S. O Halloran, M. Feeney, S. Flynn, G. Fitzgerald, C. Daly, B. Kiely, G. C. O Sullivan, F. Shanahan, and J K. Collins (2001) In vitro selection criteria for probiotic bacteria of human origin: Correlation with in vivo findings. Am. J. Clin. Nutr. 73: 386S-392S. 15. Tasi, C. C., H. Y. Hsih, H. H. Chiu, Y. Y. Lai, J. H. Liu, B. Yu (2005) Antagonistic activity against Salmonella infection in vitro and in vivo for two Lactobacillus strains from swine and poultry. Int. J. Food Microbiol. 102: Mishra, V., and D. N. Prasad (2005) Application of in vitro methods for selection of Lactobacillus casei strains as potential probiotics. Int. J. Food Microbiol. 103: Gilliland, S. E., T. E. Staley, and L. J. Bush (1984) Importance of bile tolerance of Lactobacillus acidophilus used as a dietary adjunct. J. Dairy Sci. 67: Lin, W. H., C. F. Hwangb, L. W. Chenc, and H. Y. Tsen (2006) Viable counts, characteristic evaluation for commercial lactic acid bacteria products. Food Microbiol. 23: Del, R. B. Sgorbati, M. Moglioli and D. Palenzona (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of bafidobacterium longum. Lett. Appl. Microbiol. 31: Kos, B., J. Šuškoviæ, S. Vukoviæ, M. Šimpraga, J. Frece and S. Matošiæ (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94: Malik, S., M. I. Petrova, I. J. J. Claes, T. L. A. Verhoeven, P. Busschaert, M. Vaneechoutte, B. Lievens, I. Lambrichts, R. J. Siezen, J. Balzarini, J. Vanderleyden and S. Lebeer (2013) The highly autoaggregative and adhesive phenotype of the vaginal Lactobacillus plantarum strain CMPG5300 is sortase dependent. Appl. Environ. Microbiol. 79: Kleerebezem, M., J. Boekhorst, R. van Kranenburg, D. Molenaar, O. P. Kuipers, R. Leer, R. Tarchini, S. A. Peters, H. M. Sandbrink, M. W. E. J. Fiers, W. Stiekema, R. M. K. Lankhorst, P. A. Bron, S. M. Hoffer, M. N. N. Groot, R. Kerkhoven, M. de Vries, B. Ursing, W. M. de Vos, and R. J. Siezen (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. USA 100: Ministry of Food and Drug Safety, The standard for health functional food. (2014).

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