Heterologous expression of Streptococcus mutans Cnm in Lactococcus lactis promotes intracellular invasion, adhesion to human cardiac tissues and virulence

References

• National Institutes of Health. Diagnosis and management of dental caries throughout life. NIH Consens Statement 2001; 18:1-23; PMID:11699634
   PubMedGoogle Scholar
• Bagramian RA, Garcia-Godoy F, Volpe AR. The global increase in dental caries. A pending public health crisis. Am J Dent 2009; 22:3-8; PMID:19281105
   PubMed Web of Science ®Google Scholar
• Bowen WH. The Stephan Curve revisited. Odontology 2013; 101:2-8; PMID:23224410; http://dx.doi.org/10.1007/s10266-012-0092-z
   PubMed Web of Science ®Google Scholar
• Lemos JA, Burne RA. A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology 2008; 154:3247-55; PMID:18957579; http://dx.doi.org/10.1099/mic.0.2008/023770-0
   PubMed Web of Science ®Google Scholar
• Miyatani F, Kuriyama N, Watanabe I, Nomura R, Nakano K, Matsui D, Ozaki E, Koyama T, Nishigaki M, Yamamoto T, et al. Relationship between Cnm-positive Streptococcus mutans and cerebral microbleeds in humans. Oral Dis 2015; 21:886-93; PMID:26205098; http://dx.doi.org/10.1111/odi.12360
   PubMed Web of Science ®Google Scholar
• Nakano K, Hokamura K, Taniguchi N, Wada K, Kudo C, Nomura R, Kojima A, Naka S, Muranaka Y, Thura M, et al. The collagen-binding protein of Streptococcus mutans is involved in haemorrhagic stroke. Nat Commun 2011; 2:485; PMID:21952219; http://dx.doi.org/10.1038/ncomms1491
   PubMed Web of Science ®Google Scholar
• Nomura R, Naka S, Nemoto H, Inagaki S, Taniguchi K, Ooshima T, Nakano K. Potential involvement of collagen-binding proteins of Streptococcus mutans in infective endocarditis. Oral Dis 2013; 19:387-93; PMID:22998492; http://dx.doi.org/10.1111/odi.12016
   PubMed Web of Science ®Google Scholar
• Nomura R, Nakano K, Nemoto H, Fujita K, Inagaki S, Takahashi T, Taniguchi K, Takeda M, Yoshioka H, Amano A, et al. Isolation and characterization of Streptococcus mutans in heart valve and dental plaque specimens from a patient with infective endocarditis. J Med Microbiol 2006; 55:1135-40; PMID:16849735; http://dx.doi.org/10.1099/jmm.0.46609-0
   PubMed Web of Science ®Google Scholar
• Que YA, Moreillon P. Infective endocarditis. Nat Rev Cardiol 2011; 8:322-36; PMID:21487430; http://dx.doi.org/10.1038/nrcardio.2011.43
   PubMed Web of Science ®Google Scholar
• Nakano K, Nomura R, Nakagawa I, Hamada S, Ooshima T. Demonstration of Streptococcus mutans with a cell wall polysaccharide specific to a new serotype, k, in the human oral cavity. J Clin Microbiol 2004; 42:198-202; PMID:14715753; http://dx.doi.org/10.1128/JCM.42.1.198-202.2004
   PubMed Web of Science ®Google Scholar
• Shun CT, Lu SY, Yeh CY, Chiang CP, Chia JS, Chen JY. Glucosyltransferases of viridans streptococci are modulins of interleukin-6 induction in infective endocarditis. Infect Immun 2005; 73:3261-70; PMID:15908350; http://dx.doi.org/10.1128/IAI.73.6.3261-3270.2005
   PubMed Web of Science ®Google Scholar
• Pant S, Patel NJ, Deshmukh A, Golwala H, Patel N, Badheka A, Hirsch GA, Mehta JL. Trends in infective endocarditis incidence, microbiology, and valve replacement in the United States from 2000 to 2011. J Am Coll Cardiol 2015; 65:2070-6; PMID:25975469; http://dx.doi.org/10.1016/j.jacc.2015.03.518
   PubMed Web of Science ®Google Scholar
• Murdoch DR, Corey GR, Hoen B, Miro JM, Fowler VG, Jr., Bayer AS, Karchmer AW, Olaison L, Pappas PA, Moreillon P, et al. Clinical presentation, etiology, and outcome of infective endocarditis in the 21st century: the International Collaboration on Endocarditis-Prospective Cohort Study. Arch Intern Med 2009; 169:463-73; PMID:19273776; http://dx.doi.org/10.1001/archinternmed.2008.603
   PubMed Web of Science ®Google Scholar
• Yew HS, Murdoch DR. Global trends in infective endocarditis epidemiology. Curr Infect Dis Rep 2012; 14:367-72; PMID:22592632; http://dx.doi.org/10.1007/s11908-012-0265-5
   PubMed Web of Science ®Google Scholar
• Banas JA. Virulence properties of Streptococcus mutans. Front Biosci 2004; 9:1267-77; PMID:14977543; http://dx.doi.org/10.2741/1305
   PubMed Web of Science ®Google Scholar
• Nakano K, Ooshima T. Serotype classification of Streptococcus mutans and its detection outside the oral cavity. Future Microbiol 2009; 4:891-902; PMID:19722842; http://dx.doi.org/10.2217/fmb.09.64
   PubMed Web of Science ®Google Scholar
• Oliveira FA, Forte CP, Silva PG, Lopes CB, Montenegro RC, Santos AK, Sobrinho CR, Mota MR, Sousa FB, Alves AP. Molecular analysis of oral bacteria in heart valve of patients with cardiovascular disease by real-time polymerase chain reaction. Medicine (Baltimore) 2015; 94:e2067; PMID:26632711; http://dx.doi.org/10.1097/MD.0000000000002067
   PubMed Web of Science ®Google Scholar
• Abranches J, Zeng L, Belanger M, Rodrigues PH, Simpson-Haidaris PJ, Akin D, Dunn WA, Jr., Progulske-Fox A, Burne RA. Invasion of human coronary artery endothelial cells by Streptococcus mutans OMZ175. Oral Microbiol Immunol 2009; 24:141-5; PMID:19239641; http://dx.doi.org/10.1111/j.1399-302X.2008.00487.x
   PubMedGoogle Scholar
• Aviles-Reyes A, Miller JH, Simpson-Haidaris PJ, Hagen FK, Abranches J, Lemos JA. Modification of Streptococcus mutans Cnm by PgfS contributes to adhesion, endothelial cell invasion, and virulence. J Bacteriol 2014; 196:2789-97; PMID:24837294; http://dx.doi.org/10.1128/JB.01783-14
   PubMed Web of Science ®Google Scholar
• Aviles-Reyes A, Miller JH, Simpson-Haidaris PJ, Lemos JA, Abranches J. Cnm is a major virulence factor of invasive Streptococcus mutans and part of a conserved three-gene locus. Mol Oral Microbiol 2014; 29:11-23; PMID:24103776; http://dx.doi.org/10.1111/omi.12041
   PubMed Web of Science ®Google Scholar
• Abranches J, Miller JH, Martinez AR, Simpson-Haidaris PJ, Burne RA, Lemos JA. The collagen-binding protein Cnm is required for Streptococcus mutans adherence to and intracellular invasion of human coronary artery endothelial cells. Infect Immun 2011; 79:2277-84; PMID:21422186; http://dx.doi.org/10.1128/IAI.00767-10
   PubMed Web of Science ®Google Scholar
• Nakano K, Nomura R, Taniguchi N, Lapirattanakul J, Kojima A, Naka S, Senawongse P, Srisatjaluk R, Gronroos L, Alaluusua S, et al. Molecular characterization of Streptococcus mutans strains containing the cnm gene encoding a collagen-binding adhesin. Arch Oral Biol 2010; 55:34-9; PMID:20005510; http://dx.doi.org/10.1016/j.archoralbio.2009.11.008
   PubMed Web of Science ®Google Scholar
• Nomura R, Nakano K, Taniguchi N, Lapirattanakul J, Nemoto H, Gronroos L, Alaluusua S, Ooshima T. Molecular and clinical analyses of the gene encoding the collagen-binding adhesin of Streptococcus mutans. J Med Microbiol 2009; 58:469-75; PMID:19273643; http://dx.doi.org/10.1099/jmm.0.007559-0
   PubMed Web of Science ®Google Scholar
• Naka S, Nomura R, Takashima Y, Okawa R, Ooshima T, Nakano K. A specific Streptococcus mutans strain aggravates non-alcoholic fatty liver disease. Oral Dis 2014; 20:700-6; PMID:25360469; http://dx.doi.org/10.1111/odi.12191
   PubMed Web of Science ®Google Scholar
• Mierau I, Kleerebezem M. 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. Appl Microbiol Biotechnol 2005; 68:705-17; PMID:16088349; http://dx.doi.org/10.1007/s00253-005-0107-6
   PubMed Web of Science ®Google Scholar
• Morello E, Bermudez-Humaran LG, Llull D, Sole V, Miraglio N, Langella P, Poquet I. Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 2008; 14:48-58; PMID:17957110; http://dx.doi.org/10.1159/000106082
   PubMed Web of Science ®Google Scholar
• Wyszynska A, Kobierecka P, Bardowski J, Jagusztyn-Krynicka EK. Lactic acid bacteria–20 years exploring their potential as live vectors for mucosal vaccination. Appl Microbiol Biotechnol 2015; 99:2967-77; PMID:25750046; http://dx.doi.org/10.1007/s00253-015-6498-0
   PubMed Web of Science ®Google Scholar
• Danne C, Entenza JM, Mallet A, Briandet R, Debarbouille M, Nato F, Glaser P, Jouvion G, Moreillon P, Trieu-Cuot P, et al. Molecular characterization of a Streptococcus gallolyticus genomic island encoding a pilus involved in endocarditis. J Infect Dis 2011; 204:1960-70; PMID:22043018; http://dx.doi.org/10.1093/infdis/jir666
   PubMed Web of Science ®Google Scholar
• Piroth L, Que YA, Widmer E, Panchaud A, Piu S, Entenza JM, Moreillon P. The fibrinogen- and fibronectin-binding domains of Staphylococcus aureus fibronectin-binding protein A synergistically promote endothelial invasion and experimental endocarditis. Infect Immun 2008; 76:3824-31; PMID:18541660; http://dx.doi.org/10.1128/IAI.00405-08
   PubMed Web of Science ®Google Scholar
• Que YA, Haefliger JA, Piroth L, Francois P, Widmer E, Entenza JM, Sinha B, Herrmann M, Francioli P, Vaudaux P, et al. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 2005; 201:1627-35; PMID:15897276; http://dx.doi.org/10.1084/jem.20050125
   PubMed Web of Science ®Google Scholar
• Buccato S, Maione D, Rinaudo CD, Volpini G, Taddei AR, Rosini R, Telford JL, Grandi G, Margarit I. Use of Lactococcus lactis expressing pili from group B Streptococcus as a broad-coverage vaccine against streptococcal disease. J Infect Dis 2006; 194:331-40; PMID:16826481; http://dx.doi.org/10.1086/505433
   PubMed Web of Science ®Google Scholar
• Arrecubieta C, Toba FA, von Bayern M, Akashi H, Deng MC, Naka Y, Lowy FD. SdrF, a Staphylococcus epidermidis surface protein, contributes to the initiation of ventricular assist device driveline-related infections. PLoS Pathog 2009; 5:e1000411; PMID:19412528; http://dx.doi.org/10.1371/journal.ppat.1000411
   PubMed Web of Science ®Google Scholar
• Innocentin S, Guimaraes V, Miyoshi A, Azevedo V, Langella P, Chatel JM, Lefevre F. Lactococcus lactis expressing either Staphylococcus aureus fibronectin-binding protein A or Listeria monocytogenes internalin A can efficiently internalize and deliver DNA in human epithelial cells. Appl Environ Microbiol 2009; 75:4870-8; PMID:19482952; http://dx.doi.org/10.1128/AEM.00825-09
   PubMed Web of Science ®Google Scholar
• Bryan EM, Bae T, Kleerebezem M, Dunny GM. Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 2000; 44:183-90; PMID:10964628; http://dx.doi.org/10.1006/plas.2000.1484
   PubMed Web of Science ®Google Scholar
• Holo H, Nes IF. Transformation of Lactococcus by electroporation. Methods Mol Biol 1995; 47:195-9; PMID:7550735
   PubMedGoogle Scholar
• Hayes F, Daly C, Fitzgerald GF. Identification of the minimal replicon of lactococcus lactis subsp. lactis UC317 Plasmid pCI305. Appl Environ Microbiol 1990; 56:202-9; PMID:16348092
   PubMed Web of Science ®Google Scholar
• Chuang-Smith ON, Wells CL, Henry-Stanley MJ, Dunny GM. Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS One 2010; 5:e15798; PMID:21209892; http://dx.doi.org/10.1371/journal.pone.0015798
   PubMedGoogle Scholar
• Crump KE, Bainbridge B, Brusko S, Turner LS, Ge X, Stone V, Xu P, Kitten T. The relationship of the lipoprotein SsaB, manganese and superoxide dismutase in Streptococcus sanguinis virulence for endocarditis. Mol Microbiol 2014; 92:1243-59; PMID:24750294; http://dx.doi.org/10.1111/mmi.12625
   PubMed Web of Science ®Google Scholar
• Fu RY, Chen J, Li Y. Heterologous leaky production of transglutaminase in Lactococcus lactis significantly enhances the growth performance of the host. Appl Environ Microbiol 2005; 71:8911-9; PMID:16332889; http://dx.doi.org/10.1128/AEM.71.12.8911-8919.2005
   PubMed Web of Science ®Google Scholar
• Durack DT, Beeson PB. Experimental bacterial endocarditis. I. Colonization of a sterile vegetation. Br J Exp Pathol 1972; 53:44-9; PMID:5014243
   PubMedGoogle Scholar
• Durack DT. Experimental bacterial endocarditis. IV. Structure and evolution of very early lesions. J Pathol 1975; 115:81-9; PMID:1151519; http://dx.doi.org/10.1002/path.1711150204
   PubMed Web of Science ®Google Scholar
• Miller JH, Aviles-Reyes A, Scott-Anne K, Gregoire S, Watson GE, Sampson E, Progulske-Fox A, Koo H, Bowen WH, Lemos JA, et al. The collagen binding protein Cnm contributes to oral colonization and cariogenicity of Streptococcus mutans OMZ175. Infect Immun 2015; 83:2001-10; PMID:25733523; http://dx.doi.org/10.1128/IAI.03022-14
   PubMed Web of Science ®Google Scholar
• Kojima A, Nomura R, Naka S, Okawa R, Ooshima T, Nakano K. Aggravation of inflammatory bowel diseases by oral streptococci. Oral Dis 2014; 20:359-66; PMID:23679203; http://dx.doi.org/10.1111/odi.12125
   PubMed Web of Science ®Google Scholar
• Kunji ER, Slotboom DJ, Poolman B. Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim Biophys Acta 2003; 1610:97-108; PMID:12586384; http://dx.doi.org/10.1016/S0005-2736(02)00712-5
   PubMed Web of Science ®Google Scholar
• Wegmann U, O'Connell-Motherway M, Zomer A, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson MJ, Kuipers OP, et al. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 2007; 189:3256-70; PMID:17307855; http://dx.doi.org/10.1128/JB.01768-06
   PubMed Web of Science ®Google Scholar
• Latif N, Sarathchandra P, Taylor PM, Antoniw J, Yacoub MH. Localization and pattern of expression of extracellular matrix components in human heart valves. J Heart Valve Dis 2005; 14:218-27; PMID:15792183
   PubMed Web of Science ®Google Scholar
• Rodriguez KJ, Piechura LM, Porras AM, Masters KS. Manipulation of valve composition to elucidate the role of collagen in aortic valve calcification. BMC Cardiovasc Disord 2014; 14:29; PMID:24581344; http://dx.doi.org/10.1186/1471-2261-14-29
   PubMed Web of Science ®Google Scholar
• Hinton RB, Jr., Lincoln J, Deutsch GH, Osinska H, Manning PB, Benson DW, Yutzey KE. Extracellular matrix remodeling and organization in developing and diseased aortic valves. Circ Res 2006; 98:1431-8; PMID:16645142; http://dx.doi.org/10.1161/01.RES.0000224114.65109.4e
   PubMed Web of Science ®Google Scholar
• Singh B, Fleury C, Jalalvand F, Riesbeck K. Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 2012; 36:1122-80; PMID:22537156; http://dx.doi.org/10.1111/j.1574-6976.2012.00340.x
   PubMed Web of Science ®Google Scholar
• Singh KV, La Rosa SL, Somarajan SR, Roh JH, Murray BE. The fibronectin-binding protein EfbA contributes to pathogenesis and protects against infective endocarditis caused by Enterococcus faecalis. Infect Immun 2015; 83:4487-94; PMID:26351286
   PubMed Web of Science ®Google Scholar
• Bashore TM, Cabell C, Fowler V, Jr. Update on infective endocarditis. Curr Probl Cardiol 2006; 31:274-352; PMID:16546554; http://dx.doi.org/10.1016/j.cpcardiol.2005.12.001
   PubMed Web of Science ®Google Scholar
• Nakano K, Nomura R, Nemoto H, Mukai T, Yoshioka H, Shudo Y, Hata H, Toda K, Taniguchi K, Amano A, et al. Detection of novel serotype k Streptococcus mutans in infective endocarditis patients. J Med Microbiol 2007; 56:1413-5; PMID:17893184; http://dx.doi.org/10.1099/jmm.0.47335-0
   PubMed Web of Science ®Google Scholar