Original Article
A molecular analysis of prokaryotic and viral DNA sequences in prostate tissue from patients with prostate cancer indicates the presence of multiple and diverse microorganisms
Abstract
BACKGROUND
Inflammation, both acute and chronic, is a common feature of prostate histology. While inflammation has been proposed to play an important role in both benign and malignant growth of the prostate, the stimuli for this inflammation remain poorly characterized. Infectious pathogens are potential stimuli for prostatic inflammation.
METHODS
Universal eubacterial PCR was used to test 170 prostate tissue core samples from 30 cancer patients for 16S rDNA gene sequences. Positive PCR products (n = 64, 37%) were cloned and sequenced. For comparison, tissue samples from 30 patients were cultured using standard clinical microbiological techniques. DNA samples from 200 additional patients were tested by organism‐specific PCR for the presence of Chlamydia trachomatis, Propionibacterium acnes, Trichomonas vaginalis, BK virus, Epstein–Barr virus, human cytomegalovirus, human papillomavirus, and xenotropic murine leukemia‐related virus.
RESULTS
16S sequencing results indicated the presence of 83 distinct microorganisms. Microbiological culture isolated markedly fewer species. In general, organism‐specific PCR failed to detect multiple organisms previously reported as common in the prostate. There was no significant association between the presence of particular species of bacteria and histologic evidence of acute or chronic inflammation.
CONCLUSIONS
Most prostates from men undergoing prostatectomy (87%) contain bacterial DNA from one or more species. However, the majority of individual tissue core samples were negative, suggesting regional heterogeneity in the presence of bacteria and a lack of a generalized or ubiquitous prostatic flora. Culture results suggest either the “unculturable” nature of species present in the prostate or that 16S rDNA sequences were derived from non‐viable bacteria. Prostate 68: 306–320, 2008. © 2007 Wiley‐Liss, Inc.
Citing Literature
Number of times cited according to CrossRef: 99
- Joseph Toker, Reetakshi Arora, Jennifer A. Wargo, The Microbiome in Immuno-oncology, Immunotherapy, 10.1007/978-3-030-41008-7_19, (325-334), (2020).
- Holger Brüggemann, Munir A. Al‐Zeer, Bacterial signatures and their inflammatory potentials associated with prostate cancer, APMIS, 10.1111/apm.13021, 128, 2, (80-91), (2020).
- Deborah Nejman, Ilana Livyatan, Garold Fuks, Nancy Gavert, Yaara Zwang, Leore T. Geller, Aviva Rotter-Maskowitz, Roi Weiser, Giuseppe Mallel, Elinor Gigi, Arnon Meltser, Gavin M. Douglas, Iris Kamer, Vancheswaran Gopalakrishnan, Tali Dadosh, Smadar Levin-Zaidman, Sofia Avnet, Tehila Atlan, Zachary A. Cooper, Reetakshi Arora, Alexandria P. Cogdill, Md Abdul Wadud Khan, Gabriel Ologun, Yuval Bussi, Adina Weinberger, Maya Lotan-Pompan, Ofra Golani, Gili Perry, Merav Rokah, Keren Bahar-Shany, Elisa A. Rozeman, Christian U. Blank, Anat Ronai, Ron Shaoul, Amnon Amit, Tatiana Dorfman, Ran Kremer, Zvi R. Cohen, Sagi Harnof, Tali Siegal, Einav Yehuda-Shnaidman, Einav Nili Gal-Yam, Hagit Shapira, Nicola Baldini, Morgan G. I. Langille, Alon Ben-Nun, Bella Kaufman, Aviram Nissan, Talia Golan, Maya Dadiani, Keren Levanon, Jair Bar, Shlomit Yust-Katz, Iris Barshack, Daniel S. Peeper, Dan J. Raz, Eran Segal, Jennifer A. Wargo, Judith Sandbank, Noam Shental, Ravid Straussman, The human tumor microbiome is composed of tumor type–specific intracellular bacteria, Science, 10.1126/science.aay9189, 368, 6494, (973-980), (2020).
- Kevin R. Loughlin, Commentary on characterization of urinary microbiome in patients with bladder cancer: Results from a single-institution, feasibility study, Urologic Oncology: Seminars and Original Investigations, 10.1016/j.urolonc.2020.04.001, (2020).
- James S. Lawson, Wendy K. Glenn, Evidence for a causal role by human papillomaviruses in prostate cancer – a systematic review, Infectious Agents and Cancer, 10.1186/s13027-020-00305-8, 15, 1, (2020).
- Paul Katongole, Obondo J. Sande, Moses Joloba, Steven J. Reynolds, Nixon Niyonzima, The human microbiome and its link in prostate cancer risk and pathogenesis, Infectious Agents and Cancer, 10.1186/s13027-020-00319-2, 15, 1, (2020).
- Somayeh Shatizadeh Malekshahi, Jila Yavarian, Robabeh Salehi, Farhad Babaei, Seyed Ali Ahmadi, Nastaran Ghavami, Maryam Naseri, Mostafa Hosseini, Talat Mokhtari-Azad, Nazanin-Zahra Shafiei-Jandaghi, Epstein-Barr and BK virus in cancerous and noncancerous prostate tissue, Future Virology, 10.2217/fvl-2019-0140, (2020).
- Solmaz Ohadian Moghadam, Seyed Ali Momeni, Human microbiome and prostate cancer development: current insights into the prevention and treatment, Frontiers of Medicine, 10.1007/s11684-019-0731-7, (2020).
- Johann S. de Bono, Christina Guo, Bora Gurel, Angelo M. De Marzo, Karen S. Sfanos, Ram S. Mani, Jesús Gil, Charles G. Drake, Andrea Alimonti, Prostate carcinogenesis: inflammatory storms, Nature Reviews Cancer, 10.1038/s41568-020-0267-9, (2020).
- Sarah L. Picardo, Bryan Coburn, Aaron R. Hansen, The microbiome and cancer for clinicians, Critical Reviews in Oncology/Hematology, 10.1016/j.critrevonc.2019.06.004, (2019).
- Alessia Cimadamore, Marina Scarpelli, Matteo Santoni, Francesco Massari, Francesca Tartari, Roy Cerqueti, Antonio Lopez-Beltran, Liang Cheng, Rodolfo Montironi, Genitourinary Tumors: Update on Molecular Biomarkers for Diagnosis, Prognosis and Prediction of Response to Therapy, Current Drug Metabolism, 10.2174/1389200220666190225124352, 20, 4, (305-312), (2019).
- Mark C. Markowski, Stephen A. Boorjian, Jeremy P. Burton, Noah M. Hahn, Molly A. Ingersoll, Saman Maleki Vareki, Sumanta K. Pal, Karen S. Sfanos, The Microbiome and Genitourinary Cancer: A Collaborative Review, European Urology, 10.1016/j.eururo.2018.12.043, (2019).
- Petar Bajic, Ryan A. Dornbier, Chirag P. Doshi, Alan J. Wolfe, Ahmer V. Farooq, Larissa Bresler, Implications of the Genitourinary Microbiota in Prostatic Disease, Current Urology Reports, 10.1007/s11934-019-0904-6, 20, 7, (2019).
- Babbiker Mohammed Taher Gorish, Mohammed Elfatih Hussein Ournasseir, Iman Mohammed Shammat, A correlation study of BK Polyoma Virus infection and prostate Cancer among Sudanese patients - immunofluorescence and molecular based case-control study, Infectious Agents and Cancer, 10.1186/s13027-019-0244-7, 14, 1, (2019).
- Alessia Cimadamore, Matteo Santoni, Francesco Massari, Silvia Gasparrini, Liang Cheng, Antonio Lopez-Beltran, Rodolfo Montironi, Marina Scarpelli, Microbiome and Cancers, With Focus on Genitourinary Tumors, Frontiers in Oncology, 10.3389/fonc.2019.00178, 9, (2019).
- Beth A. Helmink, M. A. Wadud Khan, Amanda Hermann, Vancheswaran Gopalakrishnan, Jennifer A. Wargo, The microbiome, cancer, and cancer therapy, Nature Medicine, 10.1038/s41591-019-0377-7, (2019).
- Manu N. Capoor, Christof Birkenmaier, Jeffrey C. Wang, Andrew McDowell, Fahad S. Ahmed, Holger Brüggemann, Erin Coscia, David G. Davies, Soren Ohrt-Nissen, Assaf Raz, Filip Ruzicka, Jonathan E. Schmitz, Vincent A. Fischetti, Ondrej Slaby, A review of microscopy-based evidence for the association of Propionibacterium acnes biofilms in degenerative disc disease and other diseased human tissue, European Spine Journal, 10.1007/s00586-019-06086-y, (2019).
- Jorge Levican, Mónica Acevedo, Oscar León, Aldo Gaggero, Francisco Aguayo, Role of BK human polyomavirus in cancer, Infectious Agents and Cancer, 10.1186/s13027-018-0182-9, 13, 1, (2018).
- Corey M. Porter, Eva Shrestha, Lauren B. Peiffer, Karen S. Sfanos, The microbiome in prostate inflammation and prostate cancer, Prostate Cancer and Prostatic Diseases, 10.1038/s41391-018-0041-1, 21, 3, (345-354), (2018).
- Heidi B. Kaplan, Justin A. Miranda, Gloria R. Gogola, Karen Gomez, Catherine G. Ambrose, Persistence of bacterial DNA in orthopedic infections, Diagnostic Microbiology and Infectious Disease, 10.1016/j.diagmicrobio.2018.01.009, 91, 2, (136-140), (2018).
- Brian Goodman, Humphrey Gardner, The microbiome and cancer, The Journal of Pathology, 10.1002/path.5047, 244, 5, (667-676), (2018).
- Eva Shrestha, James R. White, Shu-Han Yu, Ibrahim Kulac, Onur Ertunc, Angelo M. De Marzo, Srinivasan Yegnasubramanian, Leslie A. Mangold, Alan W. Partin, Karen S. Sfanos, Profiling the Urinary Microbiome in Men with Positive versus Negative Biopsies for Prostate Cancer, Journal of Urology, 10.1016/j.juro.2017.08.001, 199, 1, (161-171), (2018).
- Karen S. Sfanos, Srinivasan Yegnasubramanian, William G. Nelson, Tamara L. Lotan, Ibrahim Kulac, Jessica L. Hicks, Qizhi Zheng, Charles J. Bieberich, Michael C. Haffner, Angelo M. De Marzo, If This is True, What Does it Imply? How End-user Antibody Validation Facilitates Insights into Biology and Disease, Asian Journal of Urology, 10.1016/j.ajur.2018.11.006, (2018).
- Tongwen Ou, Michael Lilly, Wei Jiang, The Pathologic Role of Toll-Like Receptor 4 in Prostate Cancer, Frontiers in Immunology, 10.3389/fimmu.2018.01188, 9, (2018).
- Karen S. Sfanos, Srinivasan Yegnasubramanian, William G. Nelson, Angelo M. De Marzo, The inflammatory microenvironment and microbiome in prostate cancer development, Nature Reviews Urology, 10.1038/nrurol.2017.167, 15, 1, (11-24), (2017).
- Melissa Milbrandt, Anke C. Winter, Remington L. Nevin, Ratna Pakpahan, Gary Bradwin, Angelo M. De Marzo, Debra J. Elliott, Charlotte A. Gaydos, William B. Isaacs, William G. Nelson, Nader Rifai, Lori J. Sokoll, Jonathan M. Zenilman, Elizabeth A. Platz, Siobhan Sutcliffe, Insight into infection‐mediated prostate damage: Contrasting patterns of C‐reactive protein and prostate‐specific antigen levels during infection, The Prostate, 10.1002/pros.23392, 77, 13, (1325-1334), (2017).
- Merve Aydin, Aliseydi Bozkurt, Aytekin Cikman, Baris Gulhan, Mehmet Karabakan, Aysun Gokce, Murat Alper, Murat Kara, Lack of evidence of HPV etiology of prostate cancer following radical surgery and higher frequency of the Arg/Pro genotype in turkish men with prostate cancer, International braz j urol, 10.1590/s1677-5538.ibju.2015.0429, 43, 1, (36-46), (2017).
- Ilaria Cavarretta, Roberto Ferrarese, Walter Cazzaniga, Diego Saita, Roberta Lucianò, Elisa R. Ceresola, Irene Locatelli, Laura Visconti, Giovanni Lavorgna, Alberto Briganti, Manuela Nebuloni, Claudio Doglioni, Massimo Clementi, Francesco Montorsi, Filippo Canducci, Andrea Salonia, The Microbiome of the Prostate Tumor Microenvironment, European Urology, 10.1016/j.eururo.2017.03.029, 72, 4, (625-631), (2017).
- Melissa A. Yow, Sepehr N. Tabrizi, Gianluca Severi, Damien M. Bolton, John Pedersen, Graham G. Giles, Melissa C. Southey, Characterisation of microbial communities within aggressive prostate cancer tissues, Infectious Agents and Cancer, 10.1186/s13027-016-0112-7, 12, 1, (2017).
- George R. Ambalathingal, Ross S. Francis, Mark J. Smyth, Corey Smith, Rajiv Khanna, BK Polyomavirus: Clinical Aspects, Immune Regulation, and Emerging Therapies, Clinical Microbiology Reviews, 10.1128/CMR.00074-16, 30, 2, (503-528), (2017).
- Tomoya Kakegawa, Yuan Bae, Takashi Ito, Keisuke Uchida, Masaki Sekine, Yutaka Nakajima, Asuka Furukawa, Yoshimi Suzuki, Jiro Kumagai, Takumi Akashi, Yoshinobu Eishi, Frequency of Propionibacterium acnes Infection in Prostate Glands with Negative Biopsy Results Is an Independent Risk Factor for Prostate Cancer in Patients with Increased Serum PSA Titers, PLOS ONE, 10.1371/journal.pone.0169984, 12, 1, (e0169984), (2017).
- Sabina Davidsson, Jessica Carlsson, Paula Mölling, Natyra Gashi, Ove Andrén, Swen-Olof Andersson, Elzbieta Brzuszkiewicz, Anja Poehlein, Munir A. Al-Zeer, Volker Brinkmann, Carsten Scavenius, Seven Nazipi, Bo Söderquist, Holger Brüggemann, Prevalence of Flp Pili-Encoding Plasmids in Cutibacterium acnes Isolates Obtained from Prostatic Tissue, Frontiers in Microbiology, 10.3389/fmicb.2017.02241, 8, (2017).
- Joerg R. Leheste, Kathryn E. Ruvolo, Joanna E. Chrostowski, Kristin Rivera, Christopher Husko, Alyssa Miceli, Martin K. Selig, Holger Brüggemann, German Torres, P. acnes-Driven Disease Pathology: Current Knowledge and Future Directions, Frontiers in Cellular and Infection Microbiology, 10.3389/fcimb.2017.00081, 7, (2017).
- Andrea K. Miyahira, Sameek Roychowdhury, Sangeeta Goswami, Joseph E. Ippolito, Saul J. Priceman, Colin C. Pritchard, Karen S. Sfanos, Sumit K. Subudhi, Jonathan W. Simons, Kenneth J. Pienta, Howard R. Soule, Beyond Seed and Soil: Understanding and Targeting Metastatic Prostate Cancer; Report From the 2016 Coffey–Holden Prostate Cancer Academy Meeting, The Prostate, 10.1002/pros.23260, 77, 2, (123-144), (2016).
- David W. McIlwain, Marloes Zoetemelk, Jason D. Myers, Marshé T. Edwards, Brandy M. Snider, Travis J. Jerde, Coordinated induction of cell survival signaling in the inflamed microenvironment of the prostate, The Prostate, 10.1002/pros.23161, 76, 8, (722-734), (2016).
- Ying Shi, Song‐Ling Peng, Li‐Fang Yang, Xue Chen, Yong‐Guang Tao, Ya Cao, Co‐infection of Epstein‐Barr virus and human papillomavirus in human tumorigenesis, Cancer Communications, 10.1186/s40880-016-0079-1, 35, 1, (1-9), (2016).
- XIAOFENG NI, HONGZHOU MENG, FENG ZHOU, HAINING YU, JIANJIAN XIANG, SHENGRONG SHEN, Effect of hypertension on bacteria composition of prostate biopsy in patients with benign prostatic hyperplasia and prostate cancer in PSA grey-zone, Biomedical Reports, 10.3892/br.2016.655, 4, 6, (765-769), (2016).
- Sabina Davidsson, Paula Mölling, Jennifer R. Rider, Magnus Unemo, Mats G. Karlsson, Jessica Carlsson, Swen-Olof Andersson, Fredrik Elgh, Bo Söderquist, Ove Andrén, Frequency and typing of Propionibacterium acnes in prostate tissue obtained from men with and without prostate cancer, Infectious Agents and Cancer, 10.1186/s13027-016-0074-9, 11, 1, (2016).
- Siobhan Sutcliffe, Remington L. Nevin, Ratna Pakpahan, Debra J. Elliott, Marvin E. Langston, Angelo M. De Marzo, Charlotte A. Gaydos, William B. Isaacs, William G. Nelson, Lori J. Sokoll, Patrick C. Walsh, Jonathan M. Zenilman, Steven B. Cersovsky, Elizabeth A. Platz, Infectious mononucleosis, other infections and prostate‐specific antigen concentration as a marker of prostate involvement during infection, International Journal of Cancer, 10.1002/ijc.29966, 138, 9, (2221-2230), (2016).
- John R. Packer, Norman J. Maitland, The molecular and cellular origin of human prostate cancer, Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 10.1016/j.bbamcr.2016.02.016, 1863, 6, (1238-1260), (2016).
- Charurut Somboonwit, John T. Sinnott, Paul Shapshak, XMRV: Emerging Human Infection or False Alarm, Global Virology I - Identifying and Investigating Viral Diseases, 10.1007/978-1-4939-2410-3, (561-574), (2015).
- Andrew McDowell, István Nagy, Propionibacteria and Disease, Molecular Medical Microbiology, 10.1016/B978-0-12-397169-2.00046-9, (837-858), (2015).
- Jong-Myon Bae, Human papillomavirus 16 infection as a potential risk factor for prostate cancer: an adaptive meta-analysis, Epidemiology and Health, 10.4178/epih/e2015005, 37, (e2015005), (2015).
- William G. Nelson, Angelo M. DeMarzo, Srinivasan Yegnasubramanian, The Diet as a Cause of Human Prostate Cancer, Advances in Nutrition and Cancer, 10.1007/978-3-642-38007-5_4, (51-68), (2014).
- Siobhan Sutcliffe, Angelo M. De Marzo, Karen S. Sfanos, Martin Laurence, MSMB variation and prostate cancer risk: Clues towards a possible fungal etiology, The Prostate, 10.1002/pros.22778, 74, 6, (569-578), (2014).
- Ugo Moens, Marijke Van Ghelue, Bernhard Ehlers, Are human polyomaviruses co‐factors for cancers induced by other oncoviruses?, Reviews in Medical Virology, 10.1002/rmv.1798, 24, 5, (343-360), (2014).
- Vasiliki Michopoulou, Stavros P. Derdas, Emmanouil Symvoulakis, Nikolaos Mourmouras, Alexandros Nomikos, Dimitris Delakas, George Sourvinos, Demetrios A. Spandidos, Detection of human papillomavirus (HPV) DNA prevalence and p53 codon 72 (Arg72Pro) polymorphism in prostate cancer in a Greek group of patients, Tumor Biology, 10.1007/s13277-014-2604-7, 35, 12, (12765-12773), (2014).
- L. Vignozzi, G. Rastrelli, G. Corona, M. Gacci, G. Forti, M. Maggi, Benign prostatic hyperplasia: a new metabolic disease?, Journal of Endocrinological Investigation, 10.1007/s40618-014-0051-3, 37, 4, (313-322), (2014).
- Chris Cobos, José A. Figueroa, Leonardo Mirandola, Michela Colombo, Gabby Summers, Alejandro Figueroa, Amardeep Aulakh, Venu Konala, Rashmi Verma, Jehanzeb Riaz, Raymond Wade, Charles Saadeh, Rakhshanda L. Rahman, Apurva Pandey, Saba Radhi, Diane D. Nguyen, Marjorie Jenkins, Maurizio Chiriva-Internati, Everardo Cobos, The Role of Human Papilloma Virus (HPV) Infection in Non-Anogenital Cancer and the Promise of Immunotherapy: A Review, International Reviews of Immunology, 10.3109/08830185.2014.911857, 33, 5, (383-401), (2014).
- Jae-Sook Ryu, Prostatic Disease Associated with Trichomonas vaginalis , The Korean Journal of Urogenital Tract Infection and Inflammation, 10.14777/kjutii.2014.9.2.61, 9, 2, (61), (2014).
- Yuan Bae, Takashi Ito, Tadatsune Iida, Keisuke Uchida, Masaki Sekine, Yutaka Nakajima, Jiro Kumagai, Tetsuji Yokoyama, Hiroshi Kawachi, Takumi Akashi, Yoshinobu Eishi, Intracellular Propionibacterium acnes Infection in Glandular Epithelium and Stromal Macrophages of the Prostate with or without Cancer, PLoS ONE, 10.1371/journal.pone.0090324, 9, 2, (e90324), (2014).
- William G. Nelson, Karen S. Sfanos, Angelo M. DeMarzo, Srinivasan Yegnasubramanian, Prostate Inflammation and Prostate Cancer, Management of Prostate Cancer, 10.1007/978-1-60761-259-9, (103-115), (2013).
- Debika Biswal Shinohara, Ajay M. Vaghasia, Shu‐Han Yu, Tim N. Mak, Holger Brüggemann, William G. Nelson, Angelo M. De Marzo, Srinivasan Yegnasubramanian, Karen S. Sfanos, A mouse model of chronic prostatic inflammation using a human prostate cancer‐derived isolate of Propionibacterium acnes, The Prostate, 10.1002/pros.22648, 73, 9, (1007-1015), (2013).
- TS Peterson, ML Kent, JA Ferguson, VG Watral, CM Whipps, Comparison of fixatives and fixation time for PCR detection of Mycobacterium in zebrafish Danio rerio , Diseases of Aquatic Organisms, 10.3354/dao02585, 104, 2, (113-120), (2013).
- Simin D Rezaei, Anna C Hearps, John Mills, John Pedersen, Gilda Tachedjian, No association between XMRV or related gammaretroviruses in Australian prostate cancer patients, Virology Journal, 10.1186/1743-422X-10-20, 10, 1, (20), (2013).
- Natalie Fischer, Tim N. Mak, Debika Biswal Shinohara, Karen S. Sfanos, Thomas F. Meyer, Holger Brüggemann, Deciphering the Intracellular Fate of Propionibacterium acnes in Macrophages , BioMed Research International, 10.1155/2013/603046, 2013, (1-11), (2013).
- Jan Hrbacek, Michael Urban, Eva Hamsikova, Ruth Tachezy, Jiri Heracek, Thirty years of research on infection and prostate cancer: No conclusive evidence for a link. A systematic review, Urologic Oncology: Seminars and Original Investigations, 10.1016/j.urolonc.2012.01.013, 31, 7, (951-965), (2013).
- Maulilio John Kipanyula, Paul Faustin Seke Etet, Lorella Vecchio, Mohammed Farahna, Elias Nchiwan Nukenine, Armel Hervé Nwabo Kamdje, Signaling pathways bridging microbial-triggered inflammation and cancer, Cellular Signalling, 10.1016/j.cellsig.2012.10.014, 25, 2, (403-416), (2013).
- Siobhan Sutcliffe, Graham A. Colditz, Prostate cancer: is it time to expand the research focus to early-life exposures?, Nature Reviews Cancer, 10.1038/nrc3434, 13, 3, (208-518), (2013).
- Noel J. Whitaker, Wendy K. Glenn, Arisha Sahrudin, Matthew M. Orde, Warick Delprado, James S. Lawson, Human papillomavirus and Epstein Barr virus in prostate cancer: Koilocytes indicate potential oncogenic influences of human papillomavirus in prostate cancer, The Prostate, 10.1002/pros.22562, 73, 3, (236-241), (2012).
- Tim N. Mak, Shu‐Han Yu, Angelo M. De Marzo, Holger Brüggemann, Karen S. Sfanos, Multilocus sequence typing (MLST) analysis of Propionibacterium acnes isolates from radical prostatectomy specimens, The Prostate, 10.1002/pros.22621, 73, 7, (770-777), (2012).
- Tina Dalianis, Hans H. Hirsch, BK Polyomavirus and Transformation, Cancer Associated Viruses, 10.1007/978-1-4614-0016-5, (419-432), (2012).
- Karen S. Sfanos, Amanda L. Aloia, Angelo M. De Marzo, Alan Rein, XMRV and prostate cancer—a 'final' perspective, Nature Reviews Urology, 10.1038/nrurol.2011.225, 9, 2, (111-118), (2012).
- G. Q. Del Prete, M. F. Kearney, J. Spindler, A. Wiegand, E. Chertova, J. D. Roser, J. D. Estes, X. P. Hao, C. M. Trubey, A. Lara, K. Lee, C. Chaipan, J. W. Bess, K. Nagashima, B. F. Keele, R. Macallister, J. Smedley, V. K. Pathak, V. N. KewalRamani, J. M. Coffin, J. D. Lifson, Restricted Replication of Xenotropic Murine Leukemia Virus-Related Virus in Pigtailed Macaques, Journal of Virology, 10.1128/JVI.06886-11, 86, 6, (3152-3166), (2012).
- Siobhan Sutcliffe, Cathee Till, Charlotte A. Gaydos, Frank J. Jenkins, Phyllis J. Goodman, Ashraful M. Hoque, Ann W. Hsing, Ian M. Thompson, Jonathan M. Zenilman, William G. Nelson, Angelo M. De Marzo, Elizabeth A. Platz, Prospective study of cytomegalovirus serostatus and prostate cancer risk in the Prostate Cancer Prevention Trial, Cancer Causes & Control, 10.1007/s10552-012-0028-5, 23, 9, (1511-1518), (2012).
- Ping Hong, Jinming Li, Lack of evidence for a role of xenotropic murine leukemia virus-related virus in the pathogenesis of prostate cancer and/or chronic fatigue syndrome, Virus Research, 10.1016/j.virusres.2012.04.004, 167, 1, (1-7), (2012).
- Dong-Sheng Hou, Wen-Min Long, Jian Shen, Li-Ping Zhao, Xiao-Yan Pang, Chen Xu, Characterisation of the bacterial community in expressed prostatic secretions from patients with chronic prostatitis/chronic pelvic pain syndrome and infertile men: a preliminary investigation, Asian Journal of Andrology, 10.1038/aja.2012.30, 14, 4, (566-573), (2012).
- Marta Curriu, Jorge Carrillo, Marta Massanella, Elisabet Garcia, Francesc Cunyat, Ruth Peña, Peter Wienberg, Cristina Carrato, Joan Areal, Margarita Bofill, Bonaventura Clotet, Julià Blanco, Cecilia Cabrera, Susceptibility of Human Lymphoid Tissue Cultured ex vivo to Xenotropic Murine Leukemia Virus-Related Virus (XMRV) Infection, PLoS ONE, 10.1371/journal.pone.0037415, 7, 5, (e37415), (2012).
- Jaydip Das Gupta, Ka-Cheung Luk, Ning Tang, Christina Gaughan, Eric A. Klein, Eugene S. Kandel, John Hackett, Robert H. Silverman, Absence of XMRV and Closely Related Viruses in Primary Prostate Cancer Tissues Used to Derive the XMRV-Infected Cell Line 22Rv1, PLoS ONE, 10.1371/journal.pone.0036072, 7, 5, (e36072), (2012).
- Jan Olsson, Johanna Bergh Drott, Lovisa Laurantzon, Oscar Laurantzon, Anders Bergh, Fredrik Elgh, Chronic Prostatic Infection and Inflammation by Propionibacterium acnes in a Rat Prostate Infection Model, PLoS ONE, 10.1371/journal.pone.0051434, 7, 12, (e51434), (2012).
- Harriet C. T. Groom, Anne Y. Warren, David E. Neal, Kate N. Bishop, No Evidence for Infection of UK Prostate Cancer Patients with XMRV, BK Virus, Trichomonas vaginalis or Human Papilloma Viruses, PLoS ONE, 10.1371/journal.pone.0034221, 7, 3, (e34221), (2012).
- Dieter Mitteregger, Stephan W. Aberle, Athanasios Makristathis, Julia Walochnik, Wolfgang Brozek, Michael Marberger, Gero Kramer, High detection rate of Trichomonas vaginalis in benign hyperplastic prostatic tissue, Medical Microbiology and Immunology, 10.1007/s00430-011-0205-2, 201, 1, (113-116), (2011).
- Karen S Sfanos, Angelo M De Marzo, Prostate cancer and inflammation: the evidence, Histopathology, 10.1111/j.1365-2559.2011.04033.x, 60, 1, (199-215), (2011).
- Bayli J. Boehm, Sara A. Colopy, Travis J. Jerde, Christopher J. Loftus, Wade Bushman, Acute bacterial inflammation of the mouse prostate, The Prostate, 10.1002/pros.21433, 72, 3, (307-317), (2011).
- R. Hadravova, A. de Marco, P. Ulbrich, J. Stokrova, M. Dolezal, I. Pichova, T. Ruml, J. A. G. Briggs, M. Rumlova, In Vitro Assembly of Virus-Like Particles of a Gammaretrovirus, the Murine Leukemia Virus XMRV, Journal of Virology, 10.1128/JVI.05564-11, 86, 3, (1297-1306), (2011).
- Baki Akgül, David Pfister, Ruth Knüchel, Axel Heidenreich, Ulrike Wieland, Herbert Pfister, No evidence for a role of xenotropic murine leukaemia virus-related virus and BK virus in prostate cancer of German patients, Medical Microbiology and Immunology, 10.1007/s00430-011-0215-0, 201, 2, (245-248), (2011).
- Zhen-Zhen Zhang, Bao-Feng Guo, Zhuang Feng, Ling Zhang, Xue-Jian Zhao, Is XMRV a causal virus for prostate cancer?, Asian Journal of Andrology, 10.1038/aja.2011.32, 13, 5, (698-701), (2011).
- A. Katzourakis, S. Hue, P. Kellam, G. J. Towers, Phylogenetic Analysis of Murine Leukemia Virus Sequences from Longitudinally Sampled Chronic Fatigue Syndrome Patients Suggests PCR Contamination Rather than Viral Evolution, Journal of Virology, 10.1128/JVI.00827-11, 85, 20, (10909-10913), (2011).
- Vicente Soriano, XMRV, un nuevo retrovirus humano en busca de enfermedad, Medicina Clínica, 10.1016/j.medcli.2010.12.004, 136, 15, (669-670), (2011).
- David E. Kang, Michael C. Lee, Jaydip Das Gupta, Eric A. Klein, Robert H. Silverman, XMRV Discovery and Prostate Cancer-Related Research, Advances in Virology, 10.1155/2011/432837, 2011, (1-10), (2011).
- Karen S. Sfanos, John T. Isaacs, The “Infectious” Nature of Human Prostate Cancer: A Cautionary Note, Oncotarget, 10.18632/oncotarget.267, 2, 4, (281-283), (2011).
- William M. Switzer, Hongwei Jia, HaoQiang Zheng, Shaohua Tang, Walid Heneine, No Association of Xenotropic Murine Leukemia Virus-Related Viruses with Prostate Cancer, PLoS ONE, 10.1371/journal.pone.0019065, 6, 5, (e19065), (2011).
- Luis Menéndez‐Arias, Evidence and controversies on the role of XMRV in prostate cancer and chronic fatigue syndrome, Reviews in Medical Virology, 10.1002/rmv.673, 21, 1, (3-17), (2010).
- Robert H. Silverman, Carvell Nguyen, Christopher J. Weight, Eric A. Klein, The human retrovirus XMRV in prostate cancer and chronic fatigue syndrome, Nature Reviews Urology, 10.1038/nrurol.2010.77, 7, 7, (392-402), (2010).
- Margarita L Martinez-Fierro, Robin J Leach, Lauro S Gomez-Guerra, Raquel Garza-Guajardo, Teresa Johnson-Pais, Joke Beuten, Idelma B Morales-Rodriguez, Mario A Hernandez-Ordoñez, German Calderon-Cardenas, Rocio Ortiz-Lopez, Ana M Rivas-Estilla, Jesus Ancer-Rodriguez, Augusto Rojas-Martinez, Identification of viral infections in the prostate and evaluation of their association with cancer, BMC Cancer, 10.1186/1471-2407-10-326, 10, 1, (2010).
- May Khalili, Laura N. Mutton, Bora Gurel, Jessica L. Hicks, Angelo M. De Marzo, Charles J. Bieberich, Loss of Nkx3.1 Expression in Bacterial Prostatitis, The American Journal of Pathology, 10.2353/ajpath.2010.080747, 176, 5, (2259-2268), (2010).
- Siobhan Sutcliffe, Sexually transmitted infections and risk of prostate cancer: review of historical and emerging hypotheses, Future Oncology, 10.2217/fon.10.95, 6, 8, (1289-1311), (2010).
- Alice Rusmevichientong, Samson A. Chow, Biology and pathophysiology of the new human retrovirus XMRV and its association with human disease, Immunologic Research, 10.1007/s12026-010-8165-y, 48, 1-3, (27-39), (2010).
- Eu-Chang Hwang, Hyang-Sik Choi, Chang-Min Im, Seung-Il Jung, Sun-Ouck Kim, Taek-Won Kang, Dong-Deuk Kwon, Kwang-Sung Park, Soo-Bang Ryu, Prostate calculi in cancer and BPH in a cohort of Korean men: presence of calculi did not correlate with cancer risk, Asian Journal of Andrology, 10.1038/aja.2009.86, 12, 2, (215-220), (2009).
- Karen S. Sfanos, Tullia C. Bruno, Alan K. Meeker, Angelo M. De Marzo, William B. Isaacs, Charles G. Drake, Human prostate‐infiltrating CD8+ T lymphocytes are oligoclonal and PD‐1+, The Prostate, 10.1002/pros.21020, 69, 15, (1694-1703), (2009).
- Johanna R. Abend, Mengxi Jiang, Michael J. Imperiale, BK virus and human cancer: Innocent until proven guilty, Seminars in Cancer Biology, 10.1016/j.semcancer.2009.02.004, 19, 4, (252-260), (2009).
- K. S. Sfanos, B. A. Wilson, A. M. De Marzo, W. B. Isaacs, Acute inflammatory proteins constitute the organic matrix of prostatic corpora amylacea and calculi in men with prostate cancer, Proceedings of the National Academy of Sciences, 10.1073/pnas.0810473106, 106, 9, (3443-3448), (2009).
- Oleg Alexeyev, Jan Olsson, Fredrik Elgh, Is There Evidence for a Role of Propionibacterium acnes in Prostatic Disease?, Urology, 10.1016/j.urology.2008.02.052, 73, 2, (220-224), (2009).
- De-Bo Kong, Xiang-Yi Zheng, Li-Ping Xie, Ni Sima, Is prostate cancer an HPV-associated lesion?, Medical Hypotheses, 10.1016/j.mehy.2008.08.022, 72, 1, (101), (2009).
- Beverley A. Shannon, Ronald J. Cohen, Kerryn L. Garrett, Influence of 16S rDNA primer sequence mismatches on the spectrum of bacterial genera detected in prostate tissue by universal eubacterial PCR, The Prostate, 10.1002/pros.20822, 68, 14, (1487-1491), (2008).
- Karen S. Sfanos, William B. Isaacs, An evaluation of PCR primer sets used for detection of Propionibacterium acnes in prostate tissue samples, The Prostate, 10.1002/pros.20820, 68, 14, (1492-1495), (2008).
- Zeena E. Nackerdien, Perspectives on microbes as oncogenic infectious agents and implications for breast cancer, Medical Hypotheses, 10.1016/j.mehy.2008.02.016, 71, 2, (302-306), (2008).
- Nicole Fischer, Olaf Hellwinkel, Claudia Schulz, Felix K.H. Chun, Hartwig Huland, Martin Aepfelbacher, Thorsten Schlomm, Prevalence of human gammaretrovirus XMRV in sporadic prostate cancer, Journal of Clinical Virology, 10.1016/j.jcv.2008.04.016, 43, 3, (277-283), (2008).
- Siobhan Sutcliffe, Elizabeth A. Platz, Inflammation and prostate cancer: A focus on infections, Current Urology Reports, 10.1007/s11934-008-0042-z, 9, 3, (243-249), (2008).
