Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 Administration Reduces the Numbers of Candida albicans and Abundance of Enterobacteria in the Gut Microbiota of Familial Mediterranean Fever Patients
Abstract
Intestinal microorganisms play a crucial role in health and disease. The disruption of host–microbiota homeostasis has been reported to occur not only during disease development but also as a result of medication. Familial Mediterranean fever (FMF) is an inflammatory genetic disease characterized by elevated systemic reactivity against the commensal gut microbiota and high levels of Candida albicans in the gut. This study’s major objective was to investigate the effects of commercial probiotic Narine on the relative abundance of gut bacteria (specifically, enterobacteria, lactobacilli, Staphylococcus aureus, and enterococci) of C. albicans carrier and non-carrier FMF patients in remission. Our main finding indicates that the probiotic reduces numbers of C. albicans and abundance of enterobacteria in male and female patients of C. albicans carriers and non-carriers. It has pivotal effect on Enterococcus faecalis: increase in male non-carriers and decrease in female ones regardless of C. albicans status. No effect was seen for Lactobacillus and S. aureus. Our data suggest that M694V/V726A pyrin inflammasome mutations leading to FMF disease may contribute to gender-specific differences in microbial community structure in FMF patients. The study’s secondary objective was to elucidate the gender-specific differences in the gut’s microbial community of FMF patients. The tendency was detectedmore »
- Authors:
-
- Armenian National Agrarian Univ., Yerevan (Armenia). Dept. of Food Safety and Biotechnology
- International Association for Human and Animals Health Improvement, Yerevan (Armenia)
- Yerevan State Medical Univ., Yerevan (Armenia)
- Armenian National Agrarian Univ., Yerevan (Armenia)
- Kyorin Univ., Tokyo (Japan). School of Medicine
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Rutgers Univ., New Brunswick, NJ (United States). Health Promoting Naturals Lab. School of Environmental and Biological Sciences
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA), Office of Defense Nuclear Nonproliferation; International Science and Technology Center (ISTC)
- OSTI Identifier:
- 1489661
- Grant/Contract Number:
- AC02-05CH11231; A-1980; A-2134
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Immunology
- Additional Journal Information:
- Journal Volume: 9; Journal ID: ISSN 1664-3224
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; familial Mediterranean fever; M694V/V726A mutations; gut microbiota; gender; Candida albicans; Lactobacillus acidophilus INMIA 9602 Er 317/402; Enteroccocus faecalis; Enterobacteriaceae
Citation Formats
Pepoyan, Astghik, Balayan, Marine, Manvelyan, Anahit, Galstyan, Lilit, Pepoyan, Sofi, Petrosyan, Susanna, Tsaturyan, Vardan, Kamiya, Shigeru, Torok, Tamas, and Chikindas, Michael. Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 Administration Reduces the Numbers of Candida albicans and Abundance of Enterobacteria in the Gut Microbiota of Familial Mediterranean Fever Patients. United States: N. p., 2018.
Web. doi:10.3389/fimmu.2018.01426.
Pepoyan, Astghik, Balayan, Marine, Manvelyan, Anahit, Galstyan, Lilit, Pepoyan, Sofi, Petrosyan, Susanna, Tsaturyan, Vardan, Kamiya, Shigeru, Torok, Tamas, & Chikindas, Michael. Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 Administration Reduces the Numbers of Candida albicans and Abundance of Enterobacteria in the Gut Microbiota of Familial Mediterranean Fever Patients. United States. doi:10.3389/fimmu.2018.01426.
Pepoyan, Astghik, Balayan, Marine, Manvelyan, Anahit, Galstyan, Lilit, Pepoyan, Sofi, Petrosyan, Susanna, Tsaturyan, Vardan, Kamiya, Shigeru, Torok, Tamas, and Chikindas, Michael. Tue .
"Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 Administration Reduces the Numbers of Candida albicans and Abundance of Enterobacteria in the Gut Microbiota of Familial Mediterranean Fever Patients". United States. doi:10.3389/fimmu.2018.01426. https://www.osti.gov/servlets/purl/1489661.
@article{osti_1489661,
title = {Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 Administration Reduces the Numbers of Candida albicans and Abundance of Enterobacteria in the Gut Microbiota of Familial Mediterranean Fever Patients},
author = {Pepoyan, Astghik and Balayan, Marine and Manvelyan, Anahit and Galstyan, Lilit and Pepoyan, Sofi and Petrosyan, Susanna and Tsaturyan, Vardan and Kamiya, Shigeru and Torok, Tamas and Chikindas, Michael},
abstractNote = {Intestinal microorganisms play a crucial role in health and disease. The disruption of host–microbiota homeostasis has been reported to occur not only during disease development but also as a result of medication. Familial Mediterranean fever (FMF) is an inflammatory genetic disease characterized by elevated systemic reactivity against the commensal gut microbiota and high levels of Candida albicans in the gut. This study’s major objective was to investigate the effects of commercial probiotic Narine on the relative abundance of gut bacteria (specifically, enterobacteria, lactobacilli, Staphylococcus aureus, and enterococci) of C. albicans carrier and non-carrier FMF patients in remission. Our main finding indicates that the probiotic reduces numbers of C. albicans and abundance of enterobacteria in male and female patients of C. albicans carriers and non-carriers. It has pivotal effect on Enterococcus faecalis: increase in male non-carriers and decrease in female ones regardless of C. albicans status. No effect was seen for Lactobacillus and S. aureus. Our data suggest that M694V/V726A pyrin inflammasome mutations leading to FMF disease may contribute to gender-specific differences in microbial community structure in FMF patients. The study’s secondary objective was to elucidate the gender-specific differences in the gut’s microbial community of FMF patients. The tendency was detected for higher counts of enterobacteria in female FMF subjects. However, the small number of patients of these groups preclude from conclusive statements, pointing at the need for additional investigations with appropriate for statistical analysis groups of subjects involved in the study.},
doi = {10.3389/fimmu.2018.01426},
journal = {Frontiers in Immunology},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {6}
}
Web of Science
Figures / Tables:

Works referenced in this record:
Colchicine Use in Children and Adolescents With Familial Mediterranean Fever: Literature Review and Consensus Statement
journal, January 2007
- Kallinich, T.; Haffner, D.; Niehues, T.
- PEDIATRICS, Vol. 119, Issue 2
Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death
journal, May 2014
- Weng, D.; Marty-Roix, R.; Ganesan, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
Adaptive immune responses to Candida albicans infection
journal, January 2015
- Richardson, Jonathan P.; Moyes, David L.
- Virulence, Vol. 6, Issue 4
Pyrin inflammasome activation and RhoA signaling in the autoinflammatory diseases FMF and HIDS
journal, June 2016
- Park, Yong Hwan; Wood, Geryl; Kastner, Daniel L.
- Nature Immunology, Vol. 17, Issue 8
Gout-associated uric acid crystals activate the NALP3 inflammasome
journal, January 2006
- Martinon, Fabio; Pétrilli, Virginie; Mayor, Annick
- Nature, Vol. 440, Issue 7081
NLRC4 Inflammasome-Mediated Production of IL-1β Modulates Mucosal Immunity in the Lung against Gram-Negative Bacterial Infection
journal, April 2012
- Cai, Shanshan; Batra, Sanjay; Wakamatsu, Nobuko
- The Journal of Immunology, Vol. 188, Issue 11
Integrative inflammasome activity in the regulation of intestinal mucosal immune responses
journal, December 2012
- Elinav, E.; Henao-Mejia, J.; Flavell, R. A.
- Mucosal Immunology, Vol. 6, Issue 1
A Novel Role for the NLRC4 Inflammasome in Mucosal Defenses against the Fungal Pathogen Candida albicans
journal, December 2011
- Tomalka, Jeffrey; Ganesan, Sandhya; Azodi, Elaheh
- PLoS Pathogens, Vol. 7, Issue 12
Familial autoinflammation with neutrophilic dermatosis reveals a regulatory mechanism of pyrin activation
journal, March 2016
- Masters, Seth L.; Lagou, Vasiliki; Jéru, Isabelle
- Science Translational Medicine, Vol. 8, Issue 332
The regulation of MEFV expression and its role in health and familial Mediterranean fever
journal, July 2011
- Grandemange, S.; Aksentijevich, I.; Jeru, I.
- Genes & Immunity, Vol. 12, Issue 7
Triggers for Attacks in Familial Mediterranean Fever: Application of the Case-Crossover Design
journal, January 2012
- Yenokyan, G.; Armenian, H. K.
- American Journal of Epidemiology, Vol. 175, Issue 10
Candida albicans Commensalism and Pathogenicity Are Intertwined Traits Directed by a Tightly Knit Transcriptional Regulatory Circuit
journal, March 2013
- Pérez, J. Christian; Kumamoto, Carol A.; Johnson, Alexander D.
- PLoS Biology, Vol. 11, Issue 3
Estrogen decreases tight junction protein ZO-1 expression in human primary gut tissues
journal, October 2017
- Zhou, Zejun; Zhang, Lumin; Ding, Miao
- Clinical Immunology, Vol. 183
Gender Specific Differences in the Immune Response to Infection
journal, March 2011
- McClelland, Erin E.; Smith, Jennifer M.
- Archivum Immunologiae et Therapiae Experimentalis, Vol. 59, Issue 3
Inflammasomes and intestinal inflammation
journal, April 2017
- Zmora, N.; Levy, M.; Pevsner-Fishcer, M.
- Mucosal Immunology, Vol. 10, Issue 4
Potential of IL-1, IL-18 and Inflammasome Inhibition for the Treatment of Inflammatory Skin Diseases
journal, May 2017
- Fenini, Gabriele; Contassot, Emmanuel; French, Lars E.
- Frontiers in Pharmacology, Vol. 8
Fire and death: the pyrin domain joins the death-domain superfamily
journal, December 2004
- Kohl, Andreas; Grütter, Markus G.
- Comptes Rendus Biologies, Vol. 327, Issue 12
Candida albicans and Enterococcus faecalis in the gut : Synergy in commensalism?
journal, September 2013
- Garsin, Danielle A.; Lorenz, Michael C.
- Gut Microbes, Vol. 4, Issue 5
Cross-kingdom interactions: Candida albicans and bacteria
journal, October 2009
- Shirtliff, Mark E.; Peters, Brian M.; Jabra-Rizk, Mary Ann
- FEMS Microbiology Letters, Vol. 299, Issue 1
Enterobacteriaceae Act in Concert with the Gut Microbiota to Induce Spontaneous and Maternally Transmitted Colitis
journal, September 2010
- Garrett, Wendy S.; Gallini, Carey A.; Yatsunenko, Tanya
- Cell Host & Microbe, Vol. 8, Issue 3
Susceptibility to Experimental Candida albicans Urinary Tract Infection in the Rat
journal, May 1987
- Levison, M. E.; Pitsakis, P. G.
- Journal of Infectious Diseases, Vol. 155, Issue 5
Impaired immune and acute-phase responses in interleukin-6-deficient mice
journal, March 1994
- Kopf, Manfred; Baumann, Heinz; Freer, Giulia
- Nature, Vol. 368, Issue 6469
Inhibition of Cronobacter sakazakii by Lactobacillus acidophilus n.v. Er2 317/402
journal, October 2016
- Charchoghlyan, Haykuhi; Kwon, Heejun; Hwang, Dong-Ju
- Korean Journal for Food Science of Animal Resources, Vol. 36, Issue 5
Lactobacillus acidophilus INMIA 9602 Er-2 strain 317/402 probiotic regulates growth of commensal Escherichia coli in gut microbiota of familial Mediterranean fever disease subjects
journal, February 2017
- Pepoyan, A. Z.; Balayan, M. H.; Manvelyan, A. M.
- Letters in Applied Microbiology, Vol. 64, Issue 4
Correlation between age and gender in Candida species infections of complete denture wearers: a retrospective analysis
journal, January 2016
- Loster, Jolanta E.; Wieczorek, Aneta; Loster, Bartłomiej W.
- Clinical Interventions in Aging, Vol. Volume 11
MEFV-Gene Analysis in Armenian Patients with Familial Mediterranean Fever: Diagnostic Value and Unfavorable Renal Prognosis of the M694V Homozygous Genotype—Genetic and Therapeutic Implications
journal, July 1999
- Cazeneuve, Cécile; Sarkisian, Tamara; Pêcheux, Christophe
- The American Journal of Human Genetics, Vol. 65, Issue 1
The effects of hormones on sex differences in infection: from genes to behavior
journal, August 2000
- Klein, S. L.
- Neuroscience & Biobehavioral Reviews, Vol. 24, Issue 6
Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome
journal, March 2013
- Misawa, Takuma; Takahama, Michihiro; Kozaki, Tatsuya
- Nature Immunology, Vol. 14, Issue 5
Elevated Systemic Antibodies towards Commensal Gut Microbiota in Autoinflammatory Condition
journal, September 2008
- Manukyan, Gayane P.; Ghazaryan, Karine A.; Ktsoyan, Zhanna A.
- PLoS ONE, Vol. 3, Issue 9
Purification, characterisation and identification of acidocin LCHV, an antimicrobial peptide produced by Lactobacillus acidophilus n.v. Er 317/402 strain Narine
journal, March 2010
- Mkrtchyan, Hermine; Gibbons, Simon; Heidelberger, Sibylle
- International Journal of Antimicrobial Agents, Vol. 35, Issue 3
Comparing Bacterial Community Composition between Healthy and White Plague-Like Disease States in Orbicella annularis Using PhyloChip™ G3 Microarrays
journal, November 2013
- Kellogg, Christina A.; Piceno, Yvette M.; Tom, Lauren M.
- PLoS ONE, Vol. 8, Issue 11
A Yersinia Effector Protein Promotes Virulence by Preventing Inflammasome Recognition of the Type III Secretion System
journal, May 2010
- Brodsky, Igor E.; Palm, Noah W.; Sadanand, Saheli
- Cell Host & Microbe, Vol. 7, Issue 5
Increased NLRP3-dependent interleukin 1β secretion in patients with familial Mediterranean fever: correlation with MEFV genotype
journal, March 2013
- Omenetti, Alessia; Carta, Sonia; Delfino, Laura
- Annals of the Rheumatic Diseases, Vol. 73, Issue 2
Autosomal dominant familial Mediterranean fever in Northern European Caucasians associated with deletion of p.M694 residue—a case series and genetic exploration
journal, May 2016
- Rowczenio, Dorota M.; Iancu, Daniela S.; Trojer, Hadija
- Rheumatology, Vol. 56, Issue 2
The factors considered as trigger for the attacks in patients with familial Mediterranean fever
journal, July 2012
- Karadag, Omer; Tufan, Abdurrahman; Yazisiz, Veli
- Rheumatology International, Vol. 33, Issue 4
Modulation of Post-Antibiotic Bacterial Community Reassembly and Host Response by Candida albicans
journal, July 2013
- Erb Downward, John R.; Falkowski, Nicole R.; Mason, Katie L.
- Scientific Reports, Vol. 3, Issue 1
The Role of Probiotics and Prebiotics in Inducing Gut Immunity
journal, January 2013
- Vieira, Angélica T.; Teixeira, Mauro M.; Martins, Flaviano S.
- Frontiers in Immunology, Vol. 4
Approach to urinary tract infections
journal, January 2009
- Najar, Ms; Saldanha, Cl; Banday, Ka
- Indian Journal of Nephrology, Vol. 19, Issue 4
Sex Difference in Link between Interleukin-6 and Stress
journal, August 2007
- Jankord, Ryan; Turk, James R.; Schadt, James C.
- Endocrinology, Vol. 148, Issue 8
Gender differences in autoimmune disease
journal, August 2014
- Ngo, S. T.; Steyn, F. J.; McCombe, P. A.
- Frontiers in Neuroendocrinology, Vol. 35, Issue 3
Lethal tuberculosis in interleukin-6-deficient mutant mice.
journal, January 1997
- Ladel, C. H.; Blum, C.; Dreher, A.
- Infection and immunity, Vol. 65, Issue 11
Works referencing / citing this record:
Combined use of eBeam irradiation and the potential probiotic Lactobacillus rhamnosus Vahe for control of foodborne pathogen Klebsiella pneumoniae
journal, November 2019
- Balayan, Marine H.; Pepoyan, Astghik Z.; Manvelyan, Anahit M.
- Annals of Microbiology, Vol. 69, Issue 13
The piglet mycobiome during the weaning transition: a pilot study1
journal, May 2019
- Summers, Katie L.; Frey, Juli Foster; Ramsay, Timothy G.
- Journal of Animal Science, Vol. 97, Issue 7
Low-Dose Electron-Beam Irradiation for the Improvement of Biofilm Formation by Probiotic Lactobacilli
journal, June 2019
- Pepoyan, Astghik Z.; Manvelyan, Anahit M.; Balayan, Marine H.
- Probiotics and Antimicrobial Proteins, Vol. 12, Issue 2
Effects of Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 and Putative Probiotic Lactobacilli on DNA Damages in the Small Intestine of Wistar Rats In Vivo
journal, December 2018
- Pepoyan, Astghik Z.; Balayan, Marine H.; Malkhasyan, Lilit
- Probiotics and Antimicrobial Proteins, Vol. 11, Issue 3
Figures / Tables found in this record: