Journal of Indian Society of Periodontology
Journal of Indian Society of Periodontology
Home | About JISP | Search | Accepted articles | Online Early | Current Issue | Archives | Instructions | SubmissionSubscribeLogin 
Users Online: 834  Home Print this page Email this page Small font size Default font size Increase font sizeWide layoutNarrow layoutFull screen layout

   Table of Contents    
Year : 2013  |  Volume : 17  |  Issue : 6  |  Page : 700-705  

Redefining the role of dendritic cells in periodontics

Department of Periodontology, Manipal College of Dental Sciences, Manipal University, Light House Hill Road, Mangalore, Karnataka, India

Date of Submission17-Nov-2012
Date of Acceptance21-Sep-2013
Date of Web Publication7-Jan-2014

Correspondence Address:
Ashita Uppoor
Department of Periodontology, Manipal College of Dental Sciences, Manipal University, Lighthouse Hill Road, Mangalore - 575 001, Karnataka
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-124X.124467

Rights and Permissions

A properly functioning adaptive immune system signifies the best features of life. It is diverse beyond compare, tolerant without fail, and capable of behaving appropriately with a myriad of infections and other challenges. Dendritic cells (DCs) are required to explain how this remarkable system is energized and directed. DCs consist of a family of antigen presenting cells, which are bone-marrow-derived cells that patrol all tissues of the body with the possible exceptions of the brain and testes. DCs function to capture bacteria and other pathogens for processing and presentation to T cells in the secondary lymphoid organs. They serve as an essential link between innate and adaptive immune systems and induce both primary and secondary immune responses. As a result of progress worldwide, there is now evidence of a central role for dendritic cells in initiating antigen-specific immunity and tolerance. This review addresses the origins and migration of DCs to target sites, their basic biology and plasticity in playing a key role in periodontal diseases, and finally, selected strategies being pursued to harness its ability to prevent periodontal diseases.

Keywords: Dendritic cells, osteoimmunology, periodontitis, vaccine

How to cite this article:
Venkatesan G, Uppoor A, Naik DG. Redefining the role of dendritic cells in periodontics. J Indian Soc Periodontol 2013;17:700-5

How to cite this URL:
Venkatesan G, Uppoor A, Naik DG. Redefining the role of dendritic cells in periodontics. J Indian Soc Periodontol [serial online] 2013 [cited 2021 Apr 21];17:700-5. Available from:

   Introduction Top

Dendritic cells (DCs) were first described in the mid-1970s by Ralph Steinman, who observed in the spleen a subpopulation of cells with a striking dendritic shape and as potent stimulators of primary immune response. They patrol all tissues of the body with the possible exceptions of the brain and testes. During the 1970s, most immunologists considered macrophages to be the principal antigen-presenting cell (APC) in the immune system. Compared to DCs, macrophages were more abundant, were uniformly distributed throughout the body, and were known to have antigen-presenting capabilities. Since DCs are so rare, initial studies were difficult, and it was not until the 1980s that it became widely accepted that DCs were "Professional" APCs. [1]

While the rarity of DCs was a hindrance to studying them, in the 1990's, researchers learned how to generate large numbers of DCs from CD34 + bone marrow precursors or from CD14 + monocytes in vitro. The ability to expand functional DCs in vitro has increased researchers' ability to study DCs to understand mechanisms of DC interactions with the immune system and to begin to test DC therapy regiments in the clinic. [2]

In the peripheral tissues of humans, three major DC subsets have been described including two in the myeloid lineage-Langerhans cells and interstitial DC (also known as dermal DC) and the third being lymphoid or plasmacytoid DC. [3]

   Dendritic Cells in Periodontics Top

A lot of evidence has accumulated that supported the role of dentridic cells (DCs) in maintenance of oral health and possibly, in the pathogenesis of oral diseases. [4] Most of these studies identified CD1a + Langerhan cells (LCs) rather than other DC subsets. In regard to gingivitis and periodontitis, LCs increased in number in the epithelium with gingivitis, experimental gingivitis, and periodontitis. [5]

   Aggressive Periodontitis Top

The potential role of DCs in aggressive periodontitis (AP) has also been analyzed in vitro. Aggregatibacter actinomycetemcomitans (Aa), an etiological agent in localized aggressive periodontitis (LAP), appears to activate/mature DCs and induce a Th1-response. In vitro modeling has led to the hypothesis of a novel mechanism for how DCs may promote elevated IgG2 responses observed in patients with LAP. [6]

The monocytes (M) of localized juvenile periodontitis (LJP) and non-periodontitis (NP) patients mature into both macrophage (MØ) and monocyte-derived dendritic cells (MDDC), but the percentage of MDDC is more in case of LJP. The LJP monocytes secrete cytokines [Platelet-activating factor (PAF) and PGE 2 ] that selectively promote the production of IgG 2. MDDC synthesize PGE 2 in response to nanomolar concentrations of PAF while MØ makes no comparable response. Although M and MØ synthesize PAF, M accumulates more PAF than MØ; this is because when M is skewed towards MØ, there is increased activity of platelet-activating factor acetyl hydrolase (PAFAH), which decreases the level of PAF produced by MØ. The M-derived PAF acts on MDDC and leads to production of IgG 2 (protective response) and PGE 2 (causes localized destruction). Thus, the MDDC that arise from LJP monocytes promote the production of a subclass of antibody that is uniquely suited to facilitate the immune response against oral pathogens [7],[8] [Figure 1].
Figure 1: DC in aggressive periodontitis

Click here to view

Together, it is likely that the clinical impact of the MDDC is a balance between the destructive effects of inflammation and the protective effects of IgG2. A clearer understanding of the maintenance of this balance and the factors that affect it may lead to more effective treatments for severe periodontal diseases like LJP. [7]

   Chronic Periodontitis Top

LCs in the gingival epithelium are very responsive to the accumulation of bacterial plaque, migrating into the site during early gingivitis, and migrating out as the gingivitis becomes more chronic (i.e., after 21 days). [6] Another study reports, LCs decrease in epithelium with gingivitis and periodontitis. [9] This disparity is likely, due to a number of variables, including the quality of the tissue samples, the method of histophometry, the area of the gingiva being analyzed (pocket, junctional, oral, sulcular epithelia), and the 'time window' of sampling. Their increased presence in epithelium from healthy to gingivitis to periodontitis is evidenced by presence of transforming growth factor- β (TGF-β), which is required for the development of LCs in vivo and from monocytes in vitro in a higher level in the milieu of chronic periodontitis (CP). If LCs are indeed emigrating, they are being renewed by precursors continuously immigrating. One in vitro study presents the intriguing possibility that local monocytes might be the LC-precursor. These activated LCs enters lamina propria and ultimately end up in lymph nodes. [10]

   Oral Lymphoid Foci (OLF) Within Interdental Papilla Top

It is suggested that the mature DCs play a role in formation of so-called 'Oral lymphoid follicles' or lymphoid foci that develop interproximally around the teeth in periodontitis, and this is initiated in gingivitis by LCs or their progenitors homing to the epithelium in response to pathogen-associated molecular patterns (PAMP) in the oral biofilm. The LCs migration out of the epithelium may also be in response to cytokine signals for lymphoid/myeloid trafficking, i.e. epithelium/keratinocytes. These immature DCs migrate out of the gingival/pocket epithelium during chronic gingivitis, undergoing maturation as they traffic to the lymph nodes, where a T cell response is elicited [Figure 2]. This model postulates that the formation of OLF is dependent on mature DCs becoming 'stalled' within gingival lamina propria, and then these mature DCs elicit a recall T cell response locally. This implies that the OLFs are not fully developed unless and until sufficient antigenic challenge is provided by specific PAMP of pathogen/commensals in the sub-gingival flora like P. gingivalis (Pg) and F. nucleatum. To summarize, the presence of mature DCs represent that there is presence of OLF in interdental papilla. However, the presence of germinal centers, as observed in lymphoid follicles, has not yet been identified in OLF. [3],[11]
Figure 2: DC in chronic periodontitis

Click here to view

   Dendritic Cells in Linking Innate and Acquired Immunity Top

In 1992, Polly Matzinger proposed that it was the innate immune system that recognized danger and delivered non-specific signals to specific T and B cells, stimulating them as to clonally divide and differentiate into effector lymphocytes and antibody-secreting cells, respectively. Thus, the older idea that the immune system learns a complicated set of rules early in ontogeny about how to recognize self and respond only to "not self" was exchanged for a simpler model. The newer model is that professional APCs respond to the environment and carry an antigenic message to responder cells to instruct them to either develop tolerance or productive immunity. [12],[13]

A critical indirect role for DCs in B cell stimulation relate to their role in activating T cells to up-regulate CD40L and secrete B cell helper factors. However, interdigitating DCs within the paracortical areas of the lymph node can interact directly with CD40-activated naive B cells to induce proliferation through an unidentified mechanism. Furthermore, in an IL-12- dependent mechanism, DCs contribute to B cell differentiation into IgM-secreting plasma cells [14] [Figure 3].
Figure 3: DC-activating immune system

Click here to view

The interaction of T cell area DCs with B cells may be facilitated by Ebstein-Barr virus-induced molecule-1 ligand chemokine (ELC) secretion, which attracts activated B cells as well as naive T cells to the DCs microenvironment. [15] When DCs mature, they are unable to secrete polarizing cytokines such as IL-12 and undergo senescence, limiting the time frame, within which they could stimulate immunity. In summary, DCs link innate and adaptive immunity by receiving danger signals that render them capable of maturing and inducing productive immunity rather than tolerance. [2]

Also, the link between innate and adaptive immunity is explained by the fact that DCs produce IL-2. It is believed that IL-2 was exclusively produced by T cells; this made it difficult to explain how natural killer cells, part of the innate immune system, become exposed to IL-2 prior to activation of the adaptive immune response. Since DCs are capable of producing IL-2 after activation by bacteria, this IL-2 acts on natural killer cells before the IL-2, which is produced by T cell. This explains DCs role in linking innate and adaptive system [3] [Figure 4].
Figure 4: DC linking innate and adaptive immunity

Click here to view

   Immune Suppresion/Tolerance Top

Failure of migrating DCs to mature en route to the lymph nodes or the ability of DCs to depolarize cytokine profiles can lead to immune suppression/tolerance i.e., towards commensals or self-antigens. Pg lipopolysaccharide (LPS) may promote immunosuppression by this route, inducing weak DC maturation and a Th 2 bias, which is anti-inflammatory [Figure 2]. Moreover, certain Pg LPS moieties suppress DC maturation by LPS from other species. This suggests that Pg may be the proverbial 'Wolf in sheep's clothing' - appearing to the host as a commensal organism, while invading host tissue and suppressing the immune response towards other species. This characteristic of Pg is consistent with the presentation of periodontitis: Long-standing, low-grade inflammation that is difficult to resolve. Resolution of inflammation is generally favored by migration of fully matured DCs from inflamed sites into lymph nodes, where a Th 1 (inflammatory) type cell-mediated immune response can be induced. [11]

The differential localization of DC subpopulations in gingival mucosa, with immature CD1a + localized to the epithelium in health and disease and mature CD83 + DCs restricted to the T cell-rich lamina propria (LP) in CP, has been demonstrated. The presence of elevated levels of cytokines IL-1β, PGE2, and IL-10 in the local milieu of active CP suggests a counter-regulatory microenvironment supportive of DC maturation, but inhibitory of an effective cell-mediated response. In vitro evidence indicates that Pg and its LPS induce DCs to mature (through IL-1β, PGE2., etc.) but stimulate the release of counter-regulatory cytokines through IL-10 (as in vivo) and promotes an inefficient T cell response. [5]

   Role in Chronic Systemic Inflammation Top

Periodontitis appears to promote chronic inflammatory diseases, including atherosclerosis, but relevant mechanisms need clarification. Oral bacteria like Pg and Aa induce remarkable IgG responses from the host that are dominated by IgG2, and IgG2 is IFN-g-dependent and is promoted by dendritic cells (DCs). IgG2 binds not only bacteria but also oxidized LDL (oxLDL) and thus form immune complexes. LDL-reactive antibodies induced by Pg and Aa include anti-phosphorylcholine (α-PC) and β2-glycoprotein-1-dependent anti-cardiolipin (α-CL), and these antibodies may link chronic inflammatory diseases at a mechanistic level [16] [Figure 5].
Figure 5: Role in promoting chronic inflammation

Click here to view

Normal human sera contain α-PC antibodies. [17] These antibodies are primarily in the IgG2 and IgG1 subclasses and recognize both bacterial PC as well as many self-antigens, which contain PC, including platelet-activating factor (PAF), apoptotic cells, and oxLDL. [18] PC-bearing strains of Aa are capable of invading human endothelial cells via the PAF receptor, demonstrating a potential route of access to the systemic circulation for oral-bacteria-bearing PC. [19]

Anti-cardiolipin (α-CL) antibodies are characteristically found in sera of patients with anti-phospholipid syndrome (APS) and systemic lupus erythematosis. The major target antigen of autoimmune α-CL is a β2-glycoprotein-1 (β2GPI). [1] The pathogenicity of α-CL is thought to be related to its ability to interfere with the regulatory function of β2GPI in prevention of the initiation of coagulation. [20]

It has been proposed that infection with a variety of viral and bacterial pathogens can induce pathogenic α-CL via molecular mimicry. [21] These IgG antibodies bind PC or TLRVYK on oxLDL and TLRVYK-like sequences on Aa and Pg. These interactions result in ICs that bind activating-Fc receptors on DCs and promote engulfment of the ICs, antigen processing, and production of the IL-12 and IL-18 that promotes early-IFN-g production by NK cells and later by T cells in inflamed sites. Numerous pro-inflammatory chemokines and cytokines are produced by stimulated T cells and macrophages that promote atherosclerosis. Production of pro-inflammatory cytokines by macrophages is well-known, although IFN-g production is controversial [16] [Figure 5]. Proinflammatory cytokines and chemokines may up-regulate adhesion molecules on the epithelium and help sustain the influx of macrophages and other inflammatory cells. Macrophages activated by IFN-g may promote plaque destabilization. [22] Disruption of atherosclerotic plaque and thrombus formation may result in embolization that may cause myocardial infarction, stroke, or peripheral arterial occlusive disease. Thus, engagement of DCs in the sub-endothelial layer of arterial walls with α-PC/α-CL bound to microorganisms, microbial products, or oxLDL from the blood may trigger a pathway in atheromas involving DC-IL-12 production, antigen presentation, IFN-g production, macrophage activation, plaque disruption, embolization, and, ultimately, life-threatening disease. [16]
Figure 6: Plasticity of DC

Click here to view

Thus, to summarize, the Aa and Pg-induced antibodies can bind both oxLDL and oral bacteria and participate in DC-dependent mechanisms that promote inflammation. Elevated soluble-intercellular adhesion molecules are atherosclerosis-associated indicators of vascular inflammation, and these markers are elevated in AgP individuals with high α-CL. Thus, the subset of individuals with periodontitis with elevated α-CL levels may be at high risk of atherosclerosis and/or adverse pregnancy outcomes. Fortunately, serum α-PC and α-CL levels can be determined with simple blood tests, and individuals with high antibody levels may be assisted by reducing cholesterol levels to minimize atherosclerosis risk and by prenatal care to minimize adverse pregnancy outcomes. [16]

   Plasticity and Role in Osteoimmunolgy Top

A new emerging field of research, termed osteoimmunology by Arron and Choi, deals with the role of the immune system in bone remodeling. In this context, many DC subtypes can be found in the joints of patients with rheumatoid arthritis (RA) and may contribute to the exacerbated osteoclastogenesis. Santiago-Schwarz et al. have recently suggested that the inflamed RA joint controls DC growth and may be a reservoir for DC amplification and the perpetuation of DC-driven inflammatory responses. They proposed that DC contribution to osteoclastogenesis is only indirect and linked to their ability to activate naive T cells, which then produce receptor activator of NF-Kβ Ligand (RANKL) and stimulate osteoclast (OC) differentiation. [23]

Recently, a study was conducted to find the direct role of DC in osteoclast differentiation. The study demonstrates that upon proper activation by microbial or protein antigens (namely Aa, bovine insulin, and outer membrane protein-1) and during immune interactions with CD4 + T cells in vitro, DC can indeed act like OC precursors. In addition, these DC-derived OC are capable of inducing bone loss after adoptive transfer in vivo. These data suggest a direct contribution of DC during immune interactions with CD4 + T cells to inflammation-induced osteoclastogenesis [Figure 6]. These findings not only provide further evidence for DC plasticity, but also extend the current paradigm of osteoimmunology. [24]

   Fate of Dendritic Cells Top

Antigen-bearing DCs are in direct contact with naive antigen-specific T cells within the T cell areas of lymph nodes, and after interaction with T cells, these DCs are rapidly eliminated. For DC elimination to occur, activated T cells induce apoptosis of DCs by producing the TNF family molecules. The relevance of DC death after antigen presentation could be shown in patients with autoimmune lymphoproliferative syndrome (ALPS). This indicates that mature DCs presenting antigens to T cells have to be effectively eliminated in order to avoid excessive immune responses. The life span of DCs might thus be an important checkpoint to control for the induction of tolerance, priming, and chronic inflammation. [25]

   Future Directions Top

A study done by Granucci et al. used microarray technology representing 11,000 genes and expressed sequence tags (ESTs) to identify the genes that are differentially expressed upon exposure of murine DC or MØ to gram-negative bacteria (i.e. E. coli). Approximately 3,000 differentially expressed transcripts were identified, some of which conferred DC with a high T cell-stimulatory capacity relative to MØ. [26]

Although these studies used 'generic' stimulants, they provided the groundwork for more disease and pathogen-specific analysis of DC. In periodontitis, for e.g. it would be extremely important to analyze the genes on DCs (or other cells that are in direct contact with the biofilm such as epithelial cells) that are turned on or off by exposure to PAMP of the oral biofilm and associated gingival health vs. disease. [3]

The capacity of LCs and CD14 + DCs to preferentially prime cellular immunity and humoral immunity, respectively, has significant implications, most particularly in the context of novel human vaccines. Vaccines like Polio, Measles, Hepatitis B are all specific for acute infections, and their protective capacity arises largely from their induction of humoral immune responses. They principally deliver antigen to and activate CD14 + DCs but not LCs. Therefore, targeting LCs will be important for the design of vaccines that aim at eliciting strong cellular immunity. Such vaccines might be particularly useful at preventing, and perhaps even treating chronic diseases (Periodontitis) and cancer. [27],[28] Therefore, most efficient vaccines might actually be those that will target both CD14 + DCs and LCs, thereby allowing the maximal stimulation of both humoral and cellular immune responses [e.g., Smallpox, Yellow fever vaccine]. [29]

Recently, in an unpublished datum, it is stated that HA2 domain-based periodontitis vaccine was developed by Arthur Decarlo, and the results showed good immune response to HA2 immunotherapy, minimized development of periodontal disease, and was safe in animal models. [30]

   Conclusion Top

The treatment for periodontitis is emphasized more on anti-microbial, mechanical, and surgical/regenerative approaches. Even though generally effective, these treatments are generally applied after the 'damage has been done.' It would seem prudent to develop pharmacotherapeutic agents that function 'upstream' of the events that destroy the supporting tissues of the dentition. As antigen presentation through DC is the rate-limiting step in the generation of the immune/inflammatory response, blocking specific aspects of antigen presentation or the events that precede it may be a valid strategy for upstream control of periodontitis.

   References Top

1.Merad M, Manz MG, Dendritic cell homeostasis. Blood 2009;113:3418-27.  Back to cited text no. 1
2.Lipscomb MF, Masten BJ. Dendritic cells: Immune regulators in health and disease. Physiol Rev 2002;82:97-130.  Back to cited text no. 2
3.Cutler CW, Jotwani R. Antigen-presentation and role of dendritic cells in periodontics. Periodontol 2000 2004;35:135-57.  Back to cited text no. 3
4.Lombardi T, Hauser C, Budtz-Jorgensen E. Langerhans cells: Structure, function and role in oral pathological conditions. J Oral Pathol Med 1993;22:93-202.  Back to cited text no. 4
5.Jotwani R, Palucka AR, Al-Quotub M, Nouri-Shirazi M, Kim J, Bell D, et al. Mature dendritic cells infiltrate the T Cell-Rich region of oral mucosa in chronic studies periodontitis: In situ, in vivo, and in vitro. J Immunol 2001;167:4693-700.  Back to cited text no. 5
6.Cutler CW, Jotwani R. Dendritic cells at the oral mucosal interface. J Dent Res 2006;85:678-89.  Back to cited text no. 6
7.Barbour SE, Ishihara Y, Fakher M, Al-Darmaki S, Caven TH, Shelburne CP, et al. Monocyte differentiation in localized juvenile periodontitis is skewed toward the dendritic cell phenotype. Infect Immun 2002;70:2780-6.  Back to cited text no. 7
8.Al-Darmaki S, Schenkein HA, Tew JG, Barbour SE. Differential expression of platelet-activating factor acetylhydrolase in macrophages and monocyte-derived dendritic cells. J Immunol 2003;170:167-73.  Back to cited text no. 8
9.Séguier S, Godeau G, Brousse N. Immunohistological and morphometric analysis of intra- epithelial lymphocytes and Langerhans cells in healthy and diseased human gingival tissues. Arch Oral Biol 2000;45:441-52.  Back to cited text no. 9
10.Steinsvoll S, Halstensen TS, Schenck K. Extensive expression of TGF-beta1 in chronically- inflamed periodontal tissue. J Clin Periodontol 1999;26:366-73.  Back to cited text no. 10
11.Cutler CW, Teng YA. Oral mucosal dendritic cells and periodontitis: Many sides of the same coin with new twists. Periodontol 2000 2007;45:35-50.  Back to cited text no. 11
12.Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994;12:991-1045.  Back to cited text no. 12
13.Medzhitov R, janeway C Jr. Innate immunity. N Engl J Med 2000;343:338-44.  Back to cited text no. 13
14.Dubois B, Bridon JM, Fayette J, Barthelemy C, Banchereau J, Caux C, et al. Dendritic cells directly modulate B cell growth and differentiation. J Leukoc Biol 1999;66:224-30.  Back to cited text no. 14
15.Ngo VN, Tang HL, Cyster JG. Epstein-Barr virus-induced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells. J Exp Med 1998;188:181-91.  Back to cited text no. 15
16.Tew JG, El Shikh ME, El Sayed RM, Schenkein HA. Dendritic cells, Antibodies reactive with oxLDL, and Inflammation. J Dent Res 2012;91:8-16.  Back to cited text no. 16
17.Schenkein HA, Gunsolley JC, Best AM, Harrison MT, Hahn CL, Wu J, et al. Antiphosphorylcholine antibody levels are elevated in humans with periodontal diseases. Infect Immun 1999;67:4814-8.  Back to cited text no. 17
18.Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ. The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J Immunol 2003;170:6151-7.  Back to cited text no. 18
19.Schenkein HA, Barbour SE, Berry CR, Kipps B, Tew JG. Invasion of human vascular endothelial cells by Actinobacillus actinomycetemcomitans via the receptor for platelet-activating factor. Infect Immun 2000;68:5416-9.  Back to cited text no. 19
20.Mehdi AA, Uthman I, Khamashta M. Antiphospholipid syndrome: Pathogenesis and a window of treatment opportunities in the future. Eur J Clin Invest 2010;40:451-64.  Back to cited text no. 20
21.Garcia-Carrasco M, Galarza-Maldonado C, Mendoza-Pinto C, Escarcega RO, Cervera R. Infections and the antiphospholipid syndrome. Clin Rev Allergy Immunol 2009;36:104-8.  Back to cited text no. 21
22.Hansson GK, Libby P. The immune response in atherosclerosis: A double-edged sword. Nat Rev Immunol 2006;6:508-19.  Back to cited text no. 22
23.Rivollier A, Mazzorana M, Tebib J, Piperno M, Aitsiselmi T, Rabourdin-Combe C, et al. Immature dendritic cell transdifferentiation into osteoclasts: A novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 2004;104:4029-37.  Back to cited text no. 23
24.Alnaeeli M, Penninger JM, Teng YA. Immune Interactions with CD4 + T Cells Promote the Development of Functional Osteoclasts from Murine CD11c + Dendritic Cells. J Immunol 2006;177:3314-26.  Back to cited text no. 24
25.Leibbrandt A, Penninger JM. RANK/RANKL: Regulators of Immune Responses and Bone Physiology. Ann N Y Acad Sci 2008;1143:123-50.  Back to cited text no. 25
26.Granucci F, Vizzardelli C, Pavelka N, Feau S, Persico M, Virzi E, et al. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol 2001;2:882-8.  Back to cited text no. 26
27.Pulendran B, Ahmed R. Translating innate immunity into immunological memory: Implications for vaccine development. Cell 2006;124:849-63.  Back to cited text no. 27
28.Letvin NL. Correlates of Immune protection and the development of human immunodeficiency virus vaccine. Immunity 200;27:366-9.  Back to cited text no. 28
29.Frey SE, Newman FK, Cruz J, Shelton WB, Tennant JM, Polach T, et al. Dose-related effects of smallpox vaccine. N Engl J Med 2002;346:1275-80.  Back to cited text no. 29
30.Decarlo AA. Agenta Biotechnologies. Provisional Use Patent Submitted USPTO "Immunization against periodontitis with the HA2 hemoglobin binding domain of Porphyromonas gingivalis". Application number 60/529,540. Filed 12/16/2003.  Back to cited text no. 30


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  In this article
    Dendritic Cells ...
    Aggressive Perio...
    Chronic Periodon...
    Oral Lymphoid Fo...
    Dendritic Cells ...
    Immune Suppresio...
    Role in Chronic ...
    Plasticity and R...
    Fate of Dendriti...
   Future Directions
    Article Figures

 Article Access Statistics
    PDF Downloaded583    
    Comments [Add]    

Recommend this journal