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BMC Oral Health
Published in: BMC Oral Health 1/2012

Open Access 01-12-2012 | Research article

Effects of salivary protein flow and indigenous microorganisms on initial colonization of Candida albicans in an in vivo model

Authors: Norihiko Kanaguchi, Naoki Narisawa, Tatsuro Ito, Yosuke Kinoshita, Yasuka Kusumoto, Osamu Shinozuka, Hidenobu Senpuku

Published in: BMC Oral Health | Issue 1/2012

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Abstract

Background

Candida albican s is a dimorphic fungus that is part of the commensal microbial flora of the oral cavity. When the host immune defenses are impaired or when the normal microbial flora is disturbed, C. albicans triggers recurrent infections of the oral mucosa and tongue. Recently, we produced NOD/SCID.e2f1 -/- mice that show hyposalivation, decrease of salivary protein flow, lack IgA and IgG in saliva, and have decreased NK cells. Our objective was to characterize C. albicans infection and biofilm formation in mice.

Methods

NOD/SCID.e2f1 -/- mice were used as an animal model for C. albicans infection. C. albicans yeast and hyphal forms solutions were introduced in the oral cavity after disinfection by Chlorhexidine.

Results

The numbers of C. albicans colonized and decreased in a time-dependent manner in NOD/SCID.e2f1 +/+ after inoculation. However, the colonization levels were higher in NOD/SCID.e2f1 +/+ than NOD/SCID.e2f1 -/- mice. In the mice fed 1% sucrose water before inoculation, C. albicans sample was highly contaminated by indigenous microorganisms in the oral cavity; and was not in the mice fed no sucrose water. The colonization of C. albicans was not influenced by the contamination of indigenous microorganisms. The hyphal form of C. albicans restricted the restoration of indigenous microorganisms. The decreased saliva in NOD/SCID.e2f1 -/- did not increase the colonization of C. albicans in comparison to NOD/SCID.e2f1 +/+ mice. We suggest that the receptor in saliva to C. albicans may not be sufficiently provided in the oral cavity of NOD/SCID.e2f1 -/- mice.

Conclusion

The saliva protein flow may be very important for C. albicans initial colonization, where the indigenous microorganisms do not affect colonization in the oral cavity.
Appendix
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Literature
1.
Douglass LJ: Candida biofilms and their role in infection. Trends Microbiol. 2003, 11: 30-36. 10.1016/S0966-842X(02)00002-1.CrossRef
2.
Douglass LJ: Medical importance of biofilms in Candida infections. Rev Iberoam Micol. 2002, 19: 139-143.
3.
Kumamoto CA: Candida biofilms. Curr Opin Microbiol. 2002, 5: 608-611. 10.1016/S1369-5274(02)00371-5.CrossRefPubMed
4.
Kawamura-Sato K, Wachino J, Kondo T, Ito H, Arakawa Y: Reduction of disinfectant bactericidal activities in clinically isolated Actinetobacter species in the presence of organic material. J Antimicrob Chemother. 2008, 61: 568-576. 10.1093/jac/dkm498.CrossRefPubMed
5.
Lopez-Ribot JL, McAtee RK, Perea S, Kirkpatrick WP, Rinalci MG, Petterson TF: Multiple resistance phenotypes of Candida albicans coexist during episodes of oropharyngeal candidiasis in human immunodeficiency virus-infected patients. Antimicrob Agents Chemother. 1999, 43: 1621-1630.PubMedPubMedCentral
6.
Mukherjee PK, Clandra J: Candida biofilm resistance. Drug Resist Updat. 2004, 7: 301-309. 10.1016/j.drup.2004.09.002.CrossRefPubMed
7.
Ramage G, Wickes BL, Lopez-Ribot JL: Biofilms of Candida albicans and their associated resistance to antifungal agents. Am Clin Lab. 2001, 20: 42-44.PubMed
8.
Eggimann P, Garbino J, Pittet D: Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis. 2003, 3: 685-702. 10.1016/S1473-3099(03)00801-6.CrossRefPubMed
9.
Bailli GS, Douglas LJ: Matrix polymers of Candida biofilmsand their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother. 2000, 46: 397-403. 10.1093/jac/46.3.397.CrossRef
10.
Donlan RM, Costerton JW: Bioiofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002, 15: 167-193. 10.1128/CMR.15.2.167-193.2002.CrossRefPubMedPubMedCentral
11.
Kumamoto CA, Vinces MD: Alternative Candida albicans lifestyles: growth on surfaces. Annu Rev Microbiol. 2005, 59: 113-133. 10.1146/annurev.micro.59.030804.121034.CrossRefPubMed
12.
Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D: Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother. 2007, 51: 510-520. 10.1128/AAC.01056-06.CrossRefPubMed
13.
Richards MJ, Edwards JR, Culver DH, Gaynes RP: Nosocomial infections in coronary care units in the United States. National Nosocomial Infections Surveillance System. Am J Cardiol. 1998, 82: 789-793. 10.1016/S0002-9149(98)00450-0.CrossRefPubMed
14.
Reichart PA, Philipsen HP, Schmidt-Westhausen A, Samaranayake LP: Pseudomembranous oral candidiasis in HIV infection: ultrastructural findings. J Oral Pathol Med. 1995, 24: 268-281.
15.
de Repentigny L, Lewandowski D, Jolicoeur P: Immunopathogenesis of oropharyngeal candidiasis in human immunodeficiency virus infection. Clin Microbiol Rev. 2004, 17: 729-759. 10.1128/CMR.17.4.729-759.2004.CrossRefPubMedPubMedCentral
16.
Fu Y, Rieg G, Fonzi WA, Belanger PH, Edwards JE, Filler SG: Expression of the Candida albicans gene ALSI in Saccharomyces cerevisiae induces adherence to endothelial cells. Infect Immun. 1998, 66: 1783-1786.PubMedPubMedCentral
17.
McDonnell GE: Antisepsis, Disinfection, and sterilization; types, action, and resistance. 2007, Washington, DC: AZM pressCrossRef
18.
Sandovsky-Losica H, Chauhan N, Calderone R, Segal E: Gene transcription studies of Candida albicans following infection of HEp2 epithelial cells. Med Mycol. 2006, 44: 329-334. 10.1080/13693780500434701.CrossRefPubMed
19.
Cawson RA, Rajasingham KC: Ultrastructural features of the invasive phase of Candida albicans. Br J Dermatol. 1972, 87: 435-443. 10.1111/j.1365-2133.1972.tb01591.x.CrossRefPubMed
20.
Eversole LR, Reichart PA, Ficarra G, Schimidt-Westhausen A, Romagnoli P, Pimpinelli N: Oral keratinocyte immune responses in HIV-associated candidiasis. Oral Surg Oral Med Oral Pathol Oral Radiol Endodont. 1997, 84: 372-380. 10.1016/S1079-2104(97)90035-4.CrossRef
21.
Kamai Y, Kobota M, Hosokawa T, Fukuoka T, Filler SG: New model of oropharyngeal candidiasis in mice. Antimicrob Agents Chemother. 2001, 45: 3195-3197. 10.1128/AAC.45.11.3195-3197.2001.CrossRefPubMedPubMedCentral
22.
Montes LF, Wilbom WH: Ultrastructural features of host-parasite relationship in oral candidiasis. J Bacteriol. 1986, 96: 1349-1356.
23.
Matsui-Inohara H, Uematsu H, Narita T, Satoh K, Yonezawa H, Kuroda K, Ito T, Yoneda S, Kawarai T, Sugiya H, Watanabe H, Senpuku H: E2F-1-deficient NOD/SCID mice developed showing decreased saliva production. Exp Biol Med. 2009, 234: 1519-1524. 10.3181/0903-RM-115.CrossRef
24.
Ito T, Maeda T, Senpuku H: Roles of salivary components in Streptococcus mutans colonization in a new animal model using NOD/SCID.e2f1−/− mice. PLoS One. in press
25.
26.
de Repentigny L: Animal models in the analysis of Candida host-pathogen interactions. Curr Opin Microbiol. 2004, 7: 324-329. 10.1016/j.mib.2004.06.001.CrossRefPubMed
27.
Pandiyan P, Conti HR, Zheng L, Peterson AC, Mathern DR, Hernández-Santos N, Edgerton M, Gaffen SL, Lenardo MJ: Cell: CD4(+)CD25(+)Foxp3(+) regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity. 2011, 34: 422-434. 10.1016/j.immuni.2011.03.002.CrossRefPubMedPubMedCentral
28.
Matsumoto N, Salam MA, Watanabe H, Amagasa T, Senpuku H: Role of gene E2f1 in susceptibility to bacterial adherence of oral streptococci to tooth surfaces in mice. Oral Microbiol Immunol. 2004, 19: 270-276. 10.1111/j.1399-302X.2004.00151.x.CrossRefPubMed
29.
Senpuku H, Matin K, Salam MA, Kurauchi I, Sakurai S, Kawashima M, Murata T, Miyazaki H, Hanada N: Inhibitory effects of MoAbs against a surface protein antigen in real-time adherence in vitro and recolonization in vivo of Streptococcus mutans. Scand J Immunol. 2001, 54: 109-116. 10.1046/j.1365-3083.2001.00962.x.CrossRefPubMed
30.
Salam MA, Matsumoto N, Matin K, Tsuha Y, Nakao R, Hanada N, Senpuku H: Clin Diagn Lab Immunol. 2004, 11: 379-386.PubMedCentral
31.
Cannon RD, Nand AK, Jenkinson HF: Adherence of Candida albicans to human salivary components adsorbed to hydroxylapatite. Microbiology. 1995, 141: 213-219. 10.1099/00221287-141-1-213.CrossRefPubMed
32.
Nikawa H, Nishimura H, Hamada T, Yamashiro H, Samaranayake LP: Effects of modified pellicles on Candida biofilm formation on acrylic surfaces. Mycoses. 1999, 42: 37-40. 10.1046/j.1439-0507.1999.00270.x.CrossRefPubMed
33.
Nikawa H, Nishimura H, Makihira S, Hamada T, Sadamori S, Samaranayake LP: Effect of serum concentration on Candida biofilm formation on acrylic surfaces. Mycoses. 2000, 43: 139-143. 10.1046/j.1439-0507.2000.00564.x.CrossRefPubMed
34.
Tobgi RS, Samaranayake LP, MacFarlane TW: In vitro susceptibility of Candida species to lysozyme. Oral Microbiol Immunol. 1988, 3: 35-39. 10.1111/j.1399-302X.1988.tb00603.x.CrossRefPubMed
35.
Xu T, Levitz SM, Diamond RD, Oppenheim FG: Anticandidal activity of major human salivary histatins. Infect Immun. 1991, 59: 2549-2554.PubMedPubMedCentral
36.
Nikawa H, Samaranayake LP, Tenovuo J, Pang KM, Hamada T: The fungicidal effect of human lactoferrin on Candida albicans and Candida krusei. Arch Oral Biol. 1993, 38: 1057-1063. 10.1016/0003-9969(93)90167-K.CrossRefPubMed
37.
Müller F, Frøland SS, Brandtzaeg P, Fagerhol MK: Oral candidiasis is associated with low levels of parotid calprotectin in individuals with infection due to human immunodeficiency virus. Clin Infect Dis. 1993, 16: 301-302. 10.1093/clind/16.2.301.CrossRefPubMed
38.
Challacombe SJ: Immunologic aspects of oral candidiasis. Oral Surg Oral Med Oral Pathol. 1994, 78: 202-210. 10.1016/0030-4220(94)90148-1.CrossRefPubMed
39.
Samaranayake YH, MacFarlane TW, Samaranayake LP, Aitchison TC: The in vitro lysozyme susceptibility of Candida species cultured in sucrose supplemented media. J Nat Prod. 1992, 55: 1648-1654. 10.1021/np50089a014.CrossRefPubMed
40.
Cantorna MT, Balish E: Mucosal and systemic candidiasis in congenitally immunodeficient mice. Infect Immun. 1990, 58: 1093-1100.PubMedPubMedCentral
41.
Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, Huang FP, Xu D, Muller W, Moncada S, Liew FY: Altered immune responses in mice lacking inducible nitric oxide synthase. Nature. 1995, 375: 408-411. 10.1038/375408a0.CrossRefPubMed
42.
Schutte BC, Mitros JP, Bartlett JA, Walters JD, Jia HP, Welsh MJ, Casavant TL, McCray PB: Discovery of five conserved beta-defensin gene clusters using a computational search strategy. Proc Natl Acad Sci U S A. 2002, 99: 2129-2133. 10.1073/pnas.042692699.CrossRefPubMedPubMedCentral
43.
Liljemark WF, Gibbons RJ: Suppression of Candida albicans by human oral streptococci in gnotobiotic mice. Infect Immun. 1973, 8: 846-849.PubMedPubMedCentral
44.
Müller G, Kramer A: Biocompatibility index of antiseptic agents by parallel assessment of antimicrobial activity and cellular cytotoxicity. J Antimicrobial Chemother. 2008, 61: 1281-1287. 10.1093/jac/dkn125.CrossRef
45.
Sanchez IR, Nusbaum KE, Swaim SF, Hale AS, Henderson RA, McGuire JA: Chlorhexidine diacetate and povidone-iodine cytotoxicity to canine embryonic fibroblasts. Staphylococcus aureus. 1988, 17: 182-185.
46.
Grubb SE, Murdoch C, Sudbery PE, Saville SP, Lopez-Ribot JL, Thornhill MH: Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infect Immun. 2009, 77: 3872-3878. 10.1128/IAI.00518-09.CrossRefPubMedPubMedCentral
47.
Braun BR, Johnson AD: Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science. 1997, 277: 105-109. 10.1126/science.277.5322.105.CrossRefPubMed
48.
Braun BR, Head WS, Wang MX, Johnson AD: Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics. 2000, 156: 31-44.PubMedPubMedCentral
49.
Murad AM, Leng P, Straffon M, Wishart J, Macaskill S, MacCallum D, Schnell N, Talibi D, Marechal D, Tekaia F, d’Enfert C, Gaillardin C, Odds FC, Brown AJ: NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 2001, 20: 4742-4752. 10.1093/emboj/20.17.4742.CrossRefPubMedPubMedCentral
50.
Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL: Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell. 2003, 2: 1053-1060. 10.1128/EC.2.5.1053-1060.2003.CrossRefPubMedPubMedCentral
51.
Silverman RJ, Nobbs AH, Vickerman MM, Barbour ME, Jenkinson HF: Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun. 2010, 78: 4644-4652. 10.1128/IAI.00685-10.CrossRefPubMedPubMedCentral
52.
Cannon RD, Chaffin WL: Oral colonization by Candida albicans. Crit Rev Oral Biol Med. 1999, 10: 359-383. 10.1177/10454411990100030701.CrossRefPubMed
53.
Jabra-Rizk MA, Falkler WA, Merz WG, Kelley JI, Baqui AA, Meiller TF: Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J Clin Microbiol. 1999, 37: 1464-1468.PubMedPubMedCentral
54.
Chaffin WL, López-Ribot JL, Casanova M, Gozalbo D, Martínez JP: Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev. 1998, 62: 130-180.PubMedPubMedCentral
Metadata
Title
Effects of salivary protein flow and indigenous microorganisms on initial colonization of Candida albicans in an in vivo model
Authors
Norihiko Kanaguchi
Naoki Narisawa
Tatsuro Ito
Yosuke Kinoshita
Yasuka Kusumoto
Osamu Shinozuka
Hidenobu Senpuku
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2012
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/1472-6831-12-36

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