Importance of Lactobacilli for Human Health
Abstract
:1. Introduction
2. Early Gut Colonization: Sources of Lactobacilli
3. Further Steps in the Development of the Gut Microbiota
4. Lactobacilli in the Adult Gut Microbiota
5. The Role of Lactobacilli in Gut Innate and Local Immunity
6. Lactobacilli in the Vaginal Microbiota
7. Innate Immunity in the Vagina
8. Adaptive Immunity
9. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Zheng, J.; Wittouck, S.; Salvetti, E.; Franz, C.M.A.P.; Harris, H.M.B.; Mattarelli, P.; O’Toole, P.W.; Pot, B.; Vandamme, P.; Walter, J.; et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 2020, 70, 2782–2858. [Google Scholar] [CrossRef]
- O’Callaghan, J.; O’Toole, P.W. Lactobacillus: Host-microbe relationships. Curr. Top. Microbiol. Immunol. 2013, 358, 119–154. [Google Scholar]
- De Angelis, M.; Calasso, M.; Cavallo, N.; Di Cagno, R.; Gobbetti, M. Functional proteomics within the genus Lactobacillus. Proteomics 2016, 16, 946–962. [Google Scholar] [CrossRef]
- Seddik, H.A.; Bendali, F.; Gancel, F.; Fliss, I.; Spano, G.; Drider, D. Lactobacillus plantarum and Its Probiotic and Food Potentialities. Probiotics Antimicrob. Proteins 2017, 9, 111–122. [Google Scholar] [CrossRef]
- Hill, C.; Sanders, M.E. Rethinking “probiotics”. Gut Microbes 2013, 4, 269–270. [Google Scholar] [CrossRef]
- Idicula, D.V.; Krishnaprasad, N.; Parappilly, S.J.; Joy, N.; Balan, J.; George, S.M. Salutary attributes of probiotic human gut lactobacilli for gut health. Lett. Appl. Microbiol. 2023, 76, ovad011. [Google Scholar] [CrossRef]
- Thursby, E.; Juge, N. Introduction to the human gut microbiota. Biochem. J. 2017, 474, 1823–1836. [Google Scholar] [CrossRef]
- Li, J.; Jia, H.; Cai, X.; Zhong, H.; Feng, Q.; Sunagawa, S.; Arumugam, M.; Kultima, J.R.; Prifti, E.; Nielsen, T.; et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 2014, 32, 834–841. [Google Scholar] [CrossRef]
- Cavaillon, J.M.; Legout, S. Centenary of the death of Elie Metchnikoff: A visionary and an outstanding team leader. Microbes Infect. 2016, 18, 577–594. [Google Scholar] [CrossRef]
- Hornef, M.W.; Torow, N. ‘Layered immunity’ and the ‘neonatal window of opportunity’—Timed succession of non-redundant phases to establish mucosal host-microbial homeostasis after birth. Immunology 2020, 159, 15–25. [Google Scholar] [CrossRef]
- Browne, H.P.; Shao, Y.; Lawley, T.D. Mother-infant transmission of human microbiota. Curr. Opin. Microbiol. 2022, 69, 102173. [Google Scholar] [CrossRef] [PubMed]
- Bischoff, S.C.; Barbara, G.; Buurman, W.; Ockhuizen, T.; Schulzke, J.D.; Serino, M.; Tilg, H.; Watson, A.; Wells, J.M. Intestinal permeability—A new target for disease prevention and therapy. BMC Gastroenterol. 2014, 14, 189. [Google Scholar] [CrossRef]
- Strus, M.; Helwich, E.; Lauterbach, R.; Rzepecka-Węglarz, B.; Nowicka, K.; Wilińska, M.; Szczapa, J.; Rudnicka, M.; Sławska, H.; Szczepański, M.; et al. Effects of oral probiotic supplementation on gut Lactobacillus and Bifidobacterium populations and the clinical status of low-birth-weight preterm neonates: A multicenter randomized, double-blind, placebo-controlled trial. Infect. Drug Resist. 2018, 11, 1557–1571. [Google Scholar] [CrossRef]
- Golińska, E.; Strus, M.; Tomusiak-Plebanek, A.; Więcek, G.; Kozień, Ł.; Lauterbach, R.; Pawlik, D.; Rzepecka-Węglarz, B.; Kędzierska, J.; Dorycka, M.; et al. Coagulase-Negative Staphylococci Contained in Gut Microbiota as a Primary Source of Sepsis in Low- and Very Low Birth Weight Neonates. J. Clin. Med. 2020, 9, 2517. [Google Scholar] [CrossRef]
- Wójkowska-Mach, J.; Chmielarczyk, A.; Strus, M.; Lauterbach, R.; Heczko, P. Neonate Bloodstream Infections in Organization for Economic Cooperation and Development Countries: An Update on Epidemiology and Prevention. J. Clin. Med. 2019, 8, 1750. [Google Scholar] [CrossRef]
- Urushiyama, D.; Suda, W.; Ohnishi, E.; Araki, R.; Kiyoshima, C.; Kurakazu, M.; Sanui, A.; Yotsumoto, F.; Murata, M.; Nabeshima, K.; et al. Microbiome profile of the amniotic fluid as a predictive biomarker of perinatal outcome. Sci. Rep. 2017, 7, 12171. [Google Scholar] [CrossRef]
- Satokari, R.; Grönroos, T.; Laitinen, K.; Salminen, S.; Isolauri, E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett. Appl. Microbiol. 2009, 48, 8–12. [Google Scholar] [CrossRef]
- Rehbinder, E.M.; Lødrup Carlsen, K.C.; Staff, A.C.; Angell, I.L.; Landrø, L.; Hilde, K.; Gaustad, P.; Rudi, K. Is amniotic fluid of women with uncomplicated term pregnancies free of bacteria? Am. J. Obstet. Gynecol. 2018, 219, 289.e1–289.e12. [Google Scholar] [CrossRef]
- Liu, Y.; Li, X.; Zhu, B.; Zhao, H.; Ai, Q.; Tong, Y.; Qin, S.; Feng, Y.; Wang, Y.; Wang, S.; et al. Midtrimester amniotic fluid from healthy pregnancies has no microorganisms using multiple methods of microbiologic inquiry. Am. J. Obstet. Gynecol. 2020, 223, 248.e1–248.e21. [Google Scholar] [CrossRef]
- Bagg, J.; MacFarlane, T.W.; Poxton, I.R.; Smith, A.J. Essentials of Microbiology for Dental Students, 2nd ed.; Oxford University Press: Oxfordshire, UK, 2006. [Google Scholar]
- Hegde, S.; Munshi, A.K. Influence of the maternal vaginal microbiota on the oral microbiota of the newborn. J. Clin. Pediatr. Dent. 1998, 22, 317–321. [Google Scholar] [PubMed]
- Mändar, R.; Mikelsaar, M. Transmission of mother’s microflora to the newborn at birth. Biol. Neonate 1996, 69, 30–35. [Google Scholar] [CrossRef] [PubMed]
- He, Q.; Kwok, L.Y.; Xi, X.; Zhong, Z.; Ma, T.; Xu, H.; Meng, H.; Zhao, F.; Zhang, H. The meconium microbiota shares more features with the amniotic fluid microbiota than the maternal fecal and vaginal microbiota. Gut Microbes 2020, 12, 1794266. [Google Scholar] [CrossRef] [PubMed]
- Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe 2015, 17, 690–703. [Google Scholar] [CrossRef]
- Soto, A.; Martín, V.; Jiménez, E.; Mader, I.; Rodríguez, J.M.; Fernández, L. Lactobacilli and bifidobacteria in human breast milk: Influence of antibiotherapy and other host and clinical factors. J. Pediatr. Gastroenterol. Nutr. 2014, 59, 78–88. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez, J.M. The origin of human milk bacteria: Is there a bacterial entero-mammary pathway during late pregnancy and lactation? Adv. Nutr. 2014, 5, 779–784. [Google Scholar] [CrossRef]
- Lyons, K.E.; Ryan, C.A.; Dempsey, E.M.; Ross, R.P.; Stanton, C. Breast Milk, a Source of Beneficial Microbes and Associated Benefits for Infant Health. Nutrients 2020, 12, 1039. [Google Scholar] [CrossRef]
- Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971–11975. [Google Scholar] [CrossRef]
- Rinninella, E.; Raoul, P.; Cintoni, M.; Franceschi, F.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019, 7, 14. [Google Scholar] [CrossRef]
- Azad, M.A.K.; Sarker, M.; Li, T.; Yin, J. Probiotic Species in the Modulation of Gut Microbiota: An Overview. Biomed. Res. Int. 2018, 2018, 9478630. [Google Scholar] [CrossRef]
- Gupta, V.; Garg, R. Probiotics. Indian J. Med. Microbiol. 2009, 27, 202–209. [Google Scholar] [CrossRef]
- Kim, S.; Jazwinski, S.M. The Gut Microbiota and Healthy Aging: A Mini-Review. Gerontology 2018, 64, 513–520. [Google Scholar] [CrossRef]
- Mármol, I.; Sánchez-de-Diego, C.; Pradilla Dieste, A.; Cerrada, E.; Rodriguez Yoldi, M.J. Colorectal Carcinoma: A General Overview and Future Perspectives in Colorectal Cancer. Int. J. Mol. Sci. 2017, 18, 197. [Google Scholar] [CrossRef] [PubMed]
- Troost, F.J.; van Baarlen, P.; Lindsey, P.; Kodde, A.; de Vos, W.M.; Kleerebezem, M.; Brummer, R.J. Identification of the transcriptional response of human intestinal mucosa to Lactobacillus plantarum WCFS1 in vivo. BMC Genom. 2008, 9, 374. [Google Scholar] [CrossRef] [PubMed]
- van Baarlen, P.; Troost, F.J.; van Hemert, S.; van der Meer, C.; de Vos, W.M.; de Groot, P.J.; Hooiveld, G.J.; Brummer, R.J.; Kleerebezem, M. Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc. Natl. Acad. Sci. USA 2009, 106, 2371–2376. [Google Scholar] [CrossRef]
- Liu, Y.; Tian, X.; He, B.; Hoang, T.K.; Taylor, C.M.; Blanchard, E.; Freeborn, J.; Park, S.; Luo, M.; Couturier, J.; et al. Lactobacillus reuteri DSM 17938 feeding of healthy newborn mice regulates immune responses while modulating gut microbiota and boosting beneficial metabolites. Am. J. Physiol. Gastrointest. Liver Physiol. 2019, 317, G824–G838. [Google Scholar] [CrossRef] [PubMed]
- Allaire, J.M.; Crowley, S.M.; Law, H.T.; Chang, S.Y.; Ko, H.J.; Vallance, B.A. The Intestinal Epithelium: Central Coordinator of Mucosal Immunity. Trends Immunol. 2018, 39, 677–696. [Google Scholar] [CrossRef]
- Bentley, R.; Meganathan, R. Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 1982, 46, 241–280. [Google Scholar] [CrossRef]
- Plaza, S.M. The anticancer effects of vitamin K. Altern. Med. Rev. 2003, 8, 303–318. [Google Scholar]
- Rook, G.A.; Lowry, C.A.; Raison, C.L. Hygiene and other early childhood influences on the subsequent function of the immune system. Brain Res. 2015, 1617, 47–62. [Google Scholar] [CrossRef]
- Newburg, D.S. Innate immunity and human milk. J. Nutr. 2005, 135, 1308–1312. [Google Scholar] [CrossRef]
- Cheng, C.; Zhang, L.; Mu, J.; Tian, Q.; Liu, Y.; Ma, X.; Fu, Y.; Liu, Z.; Li, Z. Effect of Lactobacillus johnsonii Strain SQ0048 on the TLRs-MyD88/NF-κB Signaling Pathway in Bovine Vaginal Epithelial Cells. Front. Vet. Sci. 2021, 8, 670949. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Lü, X.; Man, C.; Han, L.; Shan, Y.; Qu, X.; Liu, Y.; Yang, S.; Xue, Y.; Zhang, Y. Lactobacillus acidophilus induces cytokine and chemokine production via NF-κB and p38 mitogen-activated protein kinase signaling pathways in intestinal epithelial cells. Clin. Vaccine Immunol. 2012, 19, 603–608. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.G.; Ohta, T.; Takahashi, T.; Kushiro, A.; Nomoto, K.; Yokokura, T.; Okada, N.; Danbara, H. Probiotic Lactobacillus casei activates innate immunity via NF-kappaB and p38 MAP kinase signaling pathways. Microbes Infect. 2006, 8, 994–1005. [Google Scholar] [CrossRef] [PubMed]
- Shin, D.; Chang, S.Y.; Bogere, P.; Won, K.; Choi, J.Y.; Choi, Y.J.; Lee, H.K.; Hur, J.; Park, B.Y.; Kim, Y.; et al. Beneficial roles of probiotics on the modulation of gut microbiota and immune response in pigs. PLoS ONE. 2019, 14, e0220843. [Google Scholar] [CrossRef] [PubMed]
- Richards, P.J.; Flaujac Lafontaine, G.M.; Connerton, P.L.; Liang, L.; Asiani, K.; Fish, N.M.; Connerton, I.F. Galacto-Oligosaccharides Modulate the Juvenile Gut Microbiome and Innate Immunity To Improve Broiler Chicken Performance. mSystems 2020, 5, e00827-19. [Google Scholar] [CrossRef]
- Forsythe, P.; Bienenstock, J. Immunomodulation by commensal and probiotic bacteria. Immunol. Investig. 2010, 39, 429–448. [Google Scholar] [CrossRef]
- Rocha-Ramírez, L.M.; Pérez-Solano, R.A.; Castañón-Alonso, S.L.; Moreno Guerrero, S.S.; Ramírez Pacheco, A.; García Garibay, M.; Eslava, C. Probiotic Lactobacillus Strains Stimulate the Inflammatory Response and Activate Human Macrophages. J. Immunol. Res. 2017, 2017, 4607491. [Google Scholar] [CrossRef]
- Marcinkiewicz, J.; Ciszek, M.; Bobek, M.; Strus, M.; Heczko, P.B.; Kurnyta, M.; Biedroń, R.; Chmielarczyk, A. Differential inflammatory mediator response in vitro from murine macrophages to lactobacilli and pathogenic intestinal bacteria. Int. J. Exp. Pathol. 2007, 88, 155–164. [Google Scholar] [CrossRef]
- Jakubczyk, D.; Leszczyńska, K.; Górska, S. The Effectiveness of Probiotics in the Treatment of Inflammatory Bowel Disease (IBD)-A Critical Review. Nutrients 2020, 12, 1973. [Google Scholar] [CrossRef]
- Ni, J.; Wu, G.D.; Albenberg, L.; Tomov, V.T. Gut microbiota and IBD: Causation or correlation? Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 573–584. [Google Scholar] [CrossRef]
- Strus, M.; Brzychczy-Włoch, M.; Kochan, P.; Heczko, P. Nadtlenek wodoru, wytwarzany przez bakterie z rodzaju Lactobacillus, jako czynnik regulujacy mikroflore pochwy [Hydrogen peroxide produced by Lactobacillus species as a regulatory molecule for vaginal microflora]. Med. Dosw. Mikrobiol. 2004, 56, 67–77. [Google Scholar] [PubMed]
- Tomusiak-Plebanek, A.; Heczko, P.; Skowron, B.; Baranowska, A.; Okoń, K.; Thor, P.J.; Strus, M. Lactobacilli with superoxide dismutase-like or catalase activity are more effective in alleviating inflammation in an inflammatory bowel disease mouse model. Drug Des. Dev. Ther. 2018, 12, 3221–3233. [Google Scholar] [CrossRef] [PubMed]
- Gevers, D.; Kugathasan, S.; Denson, L.A.; Vázquez-Baeza, Y.; Van Treuren, W.; Ren, B.; Schwager, E.; Knights, D.; Song, S.J.; Yassour, M.; et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 2014, 15, 382–392. [Google Scholar] [CrossRef] [PubMed]
- Fyderek, K.; Strus, M.; Kowalska-Duplaga, K.; Gosiewski, T.; Wedrychowicz, A.; Jedynak-Wasowicz, U.; Sładek, M.; Pieczarkowski, S.; Adamski, P.; Kochan, P.; et al. Mucosal bacterial microflora and mucus layer thickness in adolescents with inflammatory bowel disease. World J. Gastroenterol. 2009, 15, 5287–5294. [Google Scholar] [CrossRef] [PubMed]
- Pilarczyk-Zurek, M.; Chmielarczyk, A.; Gosiewski, T.; Tomusiak, A.; Adamski, P.; Zwolinska-Wcislo, M.; Mach, T.; Heczko, P.B.; Strus, M. Possible role of Escherichia coli in propagation and perpetuation of chronic inflammation in ulcerative colitis. BMC Gastroenterol. 2013, 13, 61. [Google Scholar] [CrossRef]
- Pilarczyk-Zurek, M.; Strus, M.; Adamski, P.; Heczko, P.B. The dual role of Escherichia coli in the course of ulcerative colitis. BMC Gastroenterol. 2016, 16, 128. [Google Scholar] [CrossRef]
- Liu, Y.; Fatheree, N.Y.; Mangalat, N.; Rhoads, J.M. Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-κB signaling in the intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G608–G617. [Google Scholar] [CrossRef]
- Munyaka, P.M.; Khafipour, E.; Ghia, J.E. External influence of early childhood establishment of gut microbiota and subsequent health implications. Front. Pediatr. 2014, 2, 109. [Google Scholar] [CrossRef]
- Ashraf, R.; Shah, N.P. Immune system stimulation by probiotic microorganisms. Crit. Rev. Food Sci. Nutr. 2014, 54, 938–956. [Google Scholar] [CrossRef]
- Amabebe, E.; Anumba, D.O.C. The Vaginal Microenvironment: The Physiologic Role of Lactobacilli. Front. Med. 2018, 5, 181. [Google Scholar] [CrossRef]
- Onderdonk, A.B.; Delaney, M.L.; Fichorova, R.N. The Human Microbiome during Bacterial Vaginosis. Clin. Microbiol. Rev. 2016, 29, 223–238. [Google Scholar] [CrossRef] [PubMed]
- Muzny, C.A.; Blanchard, E.; Taylor, C.M.; Aaron, K.J.; Talluri, R.; Griswold, M.E.; Redden, D.T.; Luo, M.; Welsh, D.A.; Van Der Pol, W.J.; et al. Identification of Key Bacteria Involved in the Induction of Incident Bacterial Vaginosis: A Prospective Study. J. Infect. Dis. 2018, 218, 966–978. [Google Scholar] [CrossRef] [PubMed]
- Hasan, Z.; Netherland, M.; Hasan, N.A.; Begum, N.; Yasmin, M.; Ahmed, S. An insight into the vaginal microbiome of infertile women in Bangladesh using metagenomic approach. Front. Cell. Infect. Microbiol. 2024, 14, 1390088. [Google Scholar] [CrossRef] [PubMed]
- Ravel, J.; Gajer, P.; Abdo, Z.; Schneider, G.M.; Koenig, S.S.K.; McCulle, S.L.; Karlebach, S.; Gorle, R.; Russell, J.; Tacket, C.O.; et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. USA 2011, 108, 4680–4687. [Google Scholar] [CrossRef]
- Vaneechoutte, M. The human vaginal microbial community. Res. Microbiol. 2017, 168, 811–825. [Google Scholar] [CrossRef]
- El Aila, N.A.; Tency, I.; Claeys, G.; Verstraelen, H.; Saerens, B.; Santiago, G.L.; De Backer, E.; Cools, P.; Temmerman, M.; Verhelst, R.; et al. Identification and genotyping of bacteria from paired vaginal and rectal samples from pregnant women indicates similarity between vaginal and rectal microflora. BMC Infect. Dis. 2009, 9, 167. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Gustafsson, R.J.; Ahrné, S.; Jeppsson, B.; Benoni, C.; Olsson, C.; Stjernquist, M.; Ohlsson, B. The Lactobacillus flora in vagina and rectum of fertile and postmenopausal healthy Swedish women. BMC Womens Health 2011, 11, 17. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Reid, G.; Charbonneau, D.; Erb, J.; Kochanowski, B.; Beuerman, D.; Poehner, R.; Bruce, A.W. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: Randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol. Med. Microbiol. 2003, 35, 131–134. [Google Scholar] [CrossRef]
- Heczko, P.B.; Tomusiak, A.; Adamski, P.; Jakimiuk, A.J.; Stefański, G.; Mikołajczyk-Cichońska, A.; Suda-Szczurek, M.; Strus, M. Supplementation of standard antibiotic therapy with oral probiotics for bacterial vaginosis and aerobic vaginitis: A randomised, double-blind, placebo-controlled trial. BMC Womens Health 2015, 15, 115. [Google Scholar] [CrossRef]
- Koirala, R.; Gargari, G.; Arioli, S.; Taverniti, V.; Fiore, W.; Grossi, E.; Anelli, G.M.; Cetin, I.; Guglielmetti, S. Effect of oral consumption of capsules containing Lactobacillus paracasei LPC-S01 on the vaginal microbiota of healthy adult women: A randomized, placebo-controlled, double-blind crossover study. FEMS Microbiol. Ecol. 2020, 96, fiaa084. [Google Scholar] [CrossRef]
- Witkin, S.S.; Linhares, I.M. Why do lactobacilli dominate the human vaginal microbiota? BJOG 2017, 124, 606–611. [Google Scholar] [CrossRef] [PubMed]
- Hickey, R.J.; Zhou, X.; Settles, M.L.; Erb, J.; Malone, K.; Hansmann, M.A.; Shew, M.L.; Van Der Pol, B.; Fortenberry, J.D.; Forney, L.J. Vaginal microbiota of adolescent girls prior to the onset of menarche resemble those of reproductive-age women. mBio. 2015, 6, e00097-15. [Google Scholar] [CrossRef] [PubMed]
- Neugent, M.L.; Hulyalkar, N.V.; Nguyen, V.H.; Zimmern, P.E.; De Nisco, N.J. Advances in Understanding the Human Urinary Microbiome and Its Potential Role in Urinary Tract Infection. mBio 2020, 11, e00218-20. [Google Scholar] [CrossRef]
- Zheng, D.; Liwinski, T.; Elinav, E. Interactions between microbiota and immunity in health and disease. Cell Res. 2020, 30, 492–506. [Google Scholar] [CrossRef]
- Smith, S.B.; Ravel, J. The vaginal microbiota, host defence and reproductive physiology. J. Physiol. 2017, 595, 451–463. [Google Scholar] [CrossRef] [PubMed]
- Witkin, S.S.; Linhares, I.M.; Giraldo, P. Bacterial flora of the female genital tract: Function and immune regulation. Best. Pract. Res. Clin. Obstet. Gynaecol. 2007, 21, 347–354. [Google Scholar] [CrossRef]
- Saunders, S.; Bocking, A.; Challis, J.; Reid, G. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Colloids Surf. B Biointerfaces 2007, 55, 138–142. [Google Scholar] [CrossRef]
- Axel, C.; Brosnan, B.; Zannini, E.; Peyer, L.C.; Furey, A.; Coffey, A.; Arendt, E.K. Antifungal activities of three different Lactobacillus species and their production of antifungal carboxylic acids in wheat sourdough. Appl. Microbiol. Biotechnol. 2016, 100, 1701–1711. [Google Scholar] [CrossRef]
- Szczerbiec, D.; Piechocka, J.; Głowacki, R.; Torzewska, A. Organic Acids Secreted by Lactobacillus spp. Isolated from Urine and Their Antimicrobial Activity against Uropathogenic Proteus mirabilis. Molecules 2022, 27, 5557. [Google Scholar] [CrossRef]
- Qian, Z.; Zhu, H.; Zhao, D.; Yang, P.; Gao, F.; Lu, C.; Yin, Y.; Kan, S.; Chen, D. Probiotic Lactobacillus sp. Strains Inhibit Growth, Adhesion, Biofilm Formation, and Gene Expression of Bacterial Vaginosis-Inducing Gardnerella vaginalis. Microorganisms 2021, 9, 728. [Google Scholar] [CrossRef]
- Mei, C.; Yang, W.; Wei, X.; Wu, K.; Huang, D. The Unique Microbiome and Innate Immunity During Pregnancy. Front. Immunol. 2019, 10, 2886. [Google Scholar] [CrossRef]
- McCoy, K.D.; Burkhard, R.; Geuking, M.B. The microbiome and immune memory formation. Immunol. Cell Biol. 2019, 97, 625–635. [Google Scholar] [CrossRef] [PubMed]
- Nunn, K.L.; Forney, L.J. Unraveling the dynamics of the human vaginal microbiome. Yale J. Biol. Med. 2016, 89, 331e7. [Google Scholar]
- Masson, L.; Barnabas, S.; Deese, J.; Lennard, K.; Dabee, S.; Gamieldien, H.; Jaumdally, S.Z.; Williamson, A.L.; Little, F.; Van Damme, L.; et al. Inflammatory cytokine biomarkers of asymptomatic sexually transmitted infections and vaginal dysbiosis: A multicentre validation study. Sex. Transm. Infect. 2019, 95, 5–12. [Google Scholar] [CrossRef]
- Naz, R.K. Female genital tract immunity: Distinct immunological challenges for vaccine development. J. Reprod. Immunol. 2012, 93, 1–8. [Google Scholar]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Heczko, P.B.; Giemza, M.; Ponikiewska, W.; Strus, M. Importance of Lactobacilli for Human Health. Microorganisms 2024, 12, 2382. https://doi.org/10.3390/microorganisms12122382
Heczko PB, Giemza M, Ponikiewska W, Strus M. Importance of Lactobacilli for Human Health. Microorganisms. 2024; 12(12):2382. https://doi.org/10.3390/microorganisms12122382
Chicago/Turabian StyleHeczko, Piotr B., Milena Giemza, Weronika Ponikiewska, and Magdalena Strus. 2024. "Importance of Lactobacilli for Human Health" Microorganisms 12, no. 12: 2382. https://doi.org/10.3390/microorganisms12122382
APA StyleHeczko, P. B., Giemza, M., Ponikiewska, W., & Strus, M. (2024). Importance of Lactobacilli for Human Health. Microorganisms, 12(12), 2382. https://doi.org/10.3390/microorganisms12122382