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Intracellular Porphyromonas Gingivalis Promotes the Tumorigenic Behavior of Pancreatic Carcinoma Cells

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Intracellular Porphyromonas Gingivalis Promotes the Tumorigenic Behavior of Pancreatic Carcinoma Cells cancers Article Intracellular Porphyromonas gingivalis Promotes the Tumorigenic Behavior of Pancreatic Carcinoma Cells JebaMercy Gnanasekaran 1, Adi Binder Gallimidi 1,2, Elias Saba 1, Karthikeyan Pandi 1, 1 2 1 1 1 Luba Eli Berchoer , Esther Hermano , Sarah Angabo , Hasna0a Makkawi , Arin Khashan , 1 2, , 1, , Alaa Daoud , Michael Elkin * y and Gabriel Nussbaum * y 1 The Institute of Dental Sciences, Hebrew University, Hadassah Faculty of Dental Medicine, Jerusalem 9112102, Israel; [email protected] (J.G.); [email protected] (A.B.G.); [email protected] (E.S.); [email protected] (K.P.); [email protected] (L.E.B.); [email protected] (S.A.); [email protected] (H.M.); [email protected] (A.K.); [email protected] (A.D.) 2 Sharett Oncology Institute, Hadassah-Hebrew University Medical Center, Jerusalem 9112102, Israel; [email protected] * Correspondence: [email protected] (M.E.); [email protected] (G.N.); Tel.: +972-2-6776782 (M.E.); +972-2-6758581 (G.N.) Equal contribution (these authors share the senior authorship). y Received: 2 July 2020; Accepted: 14 August 2020; Published: 18 August 2020 Abstract: Porphyromonas gingivalis is a member of the dysbiotic oral microbiome associated with oral inflammation and periodontal disease. Intriguingly, epidemiological studies link P. gingivalis to an increased risk of pancreatic cancer. Given that oral bacteria are detected in human pancreatic cancer, and both mouse and human pancreata harbor microbiota, we explored the involvement of P. gingivalis in pancreatic tumorigenesis using cell lines and a xenograft model. Live P. gingivalis induced proliferation of pancreatic cancer cells; however, surprisingly, this effect was independent of Toll-like receptor 2, the innate immune receptor that is engaged in response to P. gingivalis on other cancer and immune cells, and is required for P. gingivalis to induce alveolar bone resorption. Instead, we found that P. gingivalis survives inside pancreatic cancer cells, a trait that can be enhanced in vitro and is increased by hypoxia, a central characteristic of pancreatic cancer. Increased tumor cell proliferation was related to the degree of intracellular persistence, and infection of tumor cells with P. gingivalis led to enhanced growth in vivo. To the best of our knowledge, this study is the first to demonstrate the direct effect of exposure to P. gingivalis on the tumorigenic behavior of pancreatic cancer cell lines. Our findings shed light on potential mechanisms underlying the pancreatic cancer–periodontitis link. Keywords: Porphyromonas gingivalis; periodontitis; pancreatic neoplasms; tumor hypoxia; carcinogenesis 1. Introduction Pancreatic ductal adenocarcinoma (PDAC) is among the most aggressive and least treatable forms of cancer [1]. PDAC develops in an inflammatory environment that is present even in low-grade premalignant lesions from individuals without a history of acute or chronic pancreatitis [2]. Several studies demonstrate an association between PDAC and periodontitis, a common and chronic inflammatory disease of the oral cavity that is driven by a dysbiotic microbiome [3–5]. Periodontal disease may influence pancreatic cancer by elevating inflammatory mediators that promote tumor development, or by direct effects of bacteria on tumor cells or their microenvironment. A large, prospective, population based-study demonstrated a highly significant association between carriage of Porphyromonas gingivalis (P. gingivalis), and the risk of pancreatic cancer development [4]. P. gingivalis is Cancers 2020, 12, 2331; doi:10.3390/cancers12082331 www.mdpi.com/journal/cancers Cancers 2020, 12, x 2 of 14 Cancers 2020, 12, 2331 2 of 14 gingivalis is a gram negative, anaerobic bacteria that thrives in the inflamed environment of periodontala gram negative, lesions, anaerobic and escapes bacteria the thatbactericidal thrives inacti thevity inflamed of innate environment immune cells of periodontalby activating lesions, Toll- likeand receptor escapes the2 (TLR2) bactericidal signaling activity through of innate PI3K immune [6,7]. cellsP. gingivalis by activating is linked Toll-like to several receptor extra-oral 2 (TLR2) disorders,signaling throughand migrates PI3K to [6 tissues,7]. P. gingivalisremote fromis linked the oral to cavity several [8–13]. extra-oral Oral bacteria disorders, are andfound migrates in PDAC to samples,tissues remote and both from mouse the oral and cavity human [8–13 ].pancreata Oral bacteria harbor are foundmicrobiota in PDAC [14–17] samples,, although and both how mouse oral pathogensand human reach pancreata and invade harbor pancreatic microbiota tissue [14– 17has], althoughnot been addressed. how oral pathogens Hematogenous reach andspread invade is a likelypancreatic route tissue of access has not for been oral addressed.pathogens Hematogenoussince transient spreadbacteremia is a likelyfollows route daily of accessoral hygiene for oral procedures,pathogens since especially transient in bacteremiaindividuals follows with period daily oralontitis hygiene who procedures,harbor high especially levels of in periodontal individuals pathogenswith periodontitis [18]. Importantly, who harbor P. highgingivalis levels carriage of periodontal in the oral pathogens cavity [is18 correlated]. Importantly, with P.pancreatic gingivalis cancercarriage risk in theeven oral when cavity present is correlated years prior with to pancreatic pancreatic cancer cancer risk diagnosis even when [4], present consistent years with prior the to notionpancreatic that cancer migration diagnosis of P. [ 4gingivalis], consistent to withthe pancreas the notion from that migrationthe oral cavity, of P. gingivalis even if totransient the pancreas and intermittent,from the oral increases cavity, even cancer if transient risk. and intermittent, increases cancer risk. DespiteDespite the the epidemiological epidemiological evidence evidence implicating implicating P.P. gingivalis gingivalis inin pancreatic pancreatic tumorigenesis tumorigenesis [19], [19], thethe direct direct effects effects of of this bacterium on on PDAC PDAC tumo tumorr progression progression have have not not been been investigated, investigated, and and the the mechanismsmechanisms underlyingunderlying the theP. P. gingivalis gingivalis–PDAC–PDAC link link remain remain unclear. unclear. Here, weHere, provide we provide the first evidencethe first evidencethat P. gingivalis that P. gingivalisexerts direct exerts pro-tumorigenic direct pro-tumorigenic effects on effects pancreatic on pancreatic cancer cells.cancer Although cells. Although PDAC PDACcells are cells reported are reported to express to someexpress Toll-like some receptorsToll-like [receptors20], and P.[20], gingivalis and P.induces gingivalis proliferation induces proliferationof oral epithelial of oral tumor epithelial cells tumor in a TLR2-dependent cells in a TLR2-dependent manner [manner21], we [21], found we that found pancreatic that pancreatic tumor tumorcell proliferation cell proliferation is enhanced is enhanced by P. gingivalis by P. gingivalisindependently independently of TLR2. of SinceTLR2.P. Since gingivalis P. gingivalisis known is knownto invade to andinvade persist and inpersist epithelial in epithelial cells [22 ,cells23], we[22,23], next we addressed next addressed the hypothesis the hypothesis that P. gingivalis that P. gingivalisintracellular intracellular survival is survival linked to isits linked ability to toits promote ability to pancreatic promote tumorpancreatic cell proliferation. tumor cell proliferation. Importantly, Importantly,we found that we hypoxia, found athat dominant hypoxia, feature a dominant of the PDAC feature microenvironment of the PDAC microenvironment [24,25], greatly enhances [24,25], greatlyP. gingivalis enhancesintracellular P. gingivalis survival. intracellular To the survival. best of our To knowledge,the best of our our knowledge, study is the our first study to test is the the firstmechanistic to test the involvement mechanistic ofinvolvementP. gingivalis ofin P. pancreaticgingivalis in tumorigenesis, pancreatic tumorigene applyingsis,in applying vitro tools in andvitro a toolsxenograft and a pancreatic xenograft carcinomapancreatic modelcarcinomain vivo model. Our in results vivo. Our reveal results a previously reveal a unknownpreviously direct unknown effect directof P. gingivalis effect ofon P. PDACgingivalis progression, on PDAC highlighting progression, the highlighting importance ofthe the importance interplay betweenof the interplay hypoxia betweenand P. gingivalis hypoxiaintracellular and P. gingivalis survival intracellular in this process. survival in this process. 2.2. Results Results 2.1.2.1. P. P. gingivalis gingivalis Infection Infection Enhanc Enhanceses Pancreatic Tumor Cell Proliferation ToTo investigateinvestigate how howP. gingivalisP. gingivalisinfluences influences PDAC PDAC progression, progression, we first comparedwe first thecompared proliferation the proliferationof pancreatic of carcinoma pancreatic cell carcinoma lines in thecell absencelines in the or presence absence or of P.presence gingivalis of .P. As gingivalis shown. in As Figure shown1, inP. gingivalisFigure 1, infectionP. gingivalis significantly infection increasedsignificantly the proliferationincreased the rate proliferation of the human rate PDAC of the cell human lines PANC1PDAC celland lines MIA PANC1 PaCa-2, and and MIA the mouse PaCa-2, cell and line the Panc02. mouse cell line Panc02. FigureFigure
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