Mariana Xavier Byndloss, D.V.M., Ph.D.

Assistant Professor

mariana.x.byndloss@vumc.org
Faculty Appointments
Assistant Professor of Pathology, Microbiology and Immunology
Education
Ph.D., Veterinary Sciences, Universidade Federal de Minas Gerais , Belo Horizonte, BrazilM.V.Sc., Universidade Federal de Minas Gerais , Belo Horizonte, BrazilD.V.M., Universidade Federal de Minas Gerais , Belo Horizonte, Brazil
Office Address
A-5301A MCN
1161 21st Avenue South
Nashville, TN 37232
Research Description
In high-income countries, the leading causes of death are non-communicable diseases, such as Inflammatory Bowel Disease (IBD), cancer, and cardiovascular disease. An important feature of most non-communicable diseases is inflammation-induced gut dysbiosis characterized by a shift in the microbial community structure from obligate to facultative anaerobes such as Proteobacteria. This microbial imbalance can contribute to disease pathogenesis due to either a microbiota-derived metabolite being depleted or produced at a harmful concentration. However, little is known about the mechanism by which inflammation mediates changes in the host physiology to induce disruption of the microbial ecosystem in our large intestine leading to disease.

Our group uses a multidisciplinary approach combining microbiology, molecular biology, cell biology, immunology, and pathology to understand how inflammation-dependent changes in gut epithelial metabolism can result in gut dysbiosis and increased risk of non-communicable disease. Specifically, we used various mouse models, including diet-induced-obesity, chemical-induced colitis, and germ-free animals, to identify metabolic pathways in the gut bacteria and in the host response to microbiota-induced metabolites that will aid in the prevention of human disease.

Another arm of our research program focuses on how intestinal inflammation caused by the bacterial pathogen Salmonella enterica serovar Typhimurium induces changes in host physiology and how these changes can cause disruption of the microbial ecosystem (microbiota) in our large intestine and promote pathogen colonization and disease.

Key Questions:

How do the host and the microbiota work together to promote health?
What are the mechanisms leading to gut dysbiosis during inflammation?
Can we identify the metabolic pathways in gut bacteria and the host response to microbiota-produced metabolites that will aid in the prevention of human diseases?
Can we prevent non-communicable diseases by targeting host epithelial metabolism?
Which mechanisms are used by enteric pathogens (e.g., Salmonella Typhimurium) to overcome microbiota-mediated colonization resistance?
Research Keywords
gut microbiota; inflammation; metabolism; inflammatory bowel disease; obesity; Enterobacteriaceae; Salmonella Typhimurium; bacterial pathogenesis; Host-pathogen interactions; colonic epithelium; colon cancer
Publications
Spiga L, Fansler RT, Perera YR, Shealy NG, Munneke MJ, Torres TP, David HE, Lemoff A, Ran X, Richardson KL, Pudlo N, Martens EC, Yang ZJ, Skaar EP, Byndloss MX, Chazin WJ, Zhu W. Iron acquisition by a commensal bacterium modifies host nutritional immunity during Salmonella infection. BioRxiv. 2023 Jun 6/26/2023; PMID: 37425782, PMCID: PMC10326984, PII: 2023.06.25.546471, DOI: 10.1101/2023.06.25.546471.

Hoek KL, McClanahan KG, Latour YL, Shealy N, Piazuelo MB, Vallance BA, Byndloss MX, Wilson KT, Olivares-Villagómez D. Turicibacterales protect mice from severe Citrobacter rodentium infection. BioRxiv. 2023 Apr 4/25/2023; PMID: 37163036, PMCID: PMC10168287, PII: 2023.04.25.538270, DOI: 10.1101/2023.04.25.538270.

Jacobse J, Brown RE, Li J, Pilat JM, Pham L, Short SP, Peek CT, Rolong A, Washington MK, Martinez-Barricarte R, Byndloss MX, Shelton C, Markle JG, Latour YL, Allaman MM, Cassat JE, Wilson KT, Choksi YA, Williams CS, Lau KS, Flynn CR, Casanova JL, Rings EHHM, Samsom JN, Goettel JA. Interleukin-23 receptor signaling impairs the stability and function of colonic regulatory T cells. Cell Rep [print-electronic]. 2023 Feb 2/17/2023; 42(2): 112128. PMID: 36807140, PII: S2211-1247(23)00139-0, DOI: 10.1016/j.celrep.2023.112128, ISSN: 2211-1247.

Lunnemann HM, Shealy NG, Reyzer ML, Shupe JA, Green EH, Siddiqi U, Lacy DB, Byndloss MX, Markham NO. Cecum axis (CecAx) preservation reveals physiological and pathological gradients in mouse gastrointestinal epithelium. Gut Microbes. 2023; 15(1): 2185029. PMID: 36872510, PMCID: PMC10012889, DOI: 10.1080/19490976.2023.2185029, ISSN: 1949-0984.

Liou MJ, Miller BM, Litvak Y, Nguyen H, Natwick DE, Savage HP, Rixon JA, Mahan SP, Hiyoshi H, Rogers AWL, Velazquez EM, Butler BP, Collins SR, McSorley SJ, Harshey RM, Byndloss MX, Simon SI, Bäumler AJ. Host cells subdivide nutrient niches into discrete biogeographical microhabitats for gut microbes. Cell Host Microbe [print-electronic]. 2022 Jun 6/8/2022; 30(6): 836-847.e6. PMID: 35568027, PMCID: PMC9187619, PII: S1931-3128(22)00218-9, DOI: 10.1016/j.chom.2022.04.012, ISSN: 1934-6069.

Tsai AY, Byndloss MX, Seyffert N, Winter MG, Young BM, Tsolis RM. Tumor Necrosis Factor Alpha Contributes to Inflammatory Pathology in the Placenta during Brucella abortus Infection. Infect Immun [print-electronic]. 2022 Mar 3/17/2022; 90(3): e0001322. PMID: 35100011, PMCID: PMC8929372, DOI: 10.1128/iai.00013-22, ISSN: 1098-5522.

Eng C, Jácome AA, Agarwal R, Hayat MH, Byndloss MX, Holowatyj AN, Bailey C, Lieu CH. A comprehensive framework for early-onset colorectal cancer research. Lancet Oncol [print-electronic]. 2022 Mar; 23(3): e116-e128. PMID: 35090673, PII: S1470-2045(21)00588-X, DOI: 10.1016/S1470-2045(21)00588-X, ISSN: 1474-5488.

Shelton CD, Yoo W, Shealy NG, Torres TP, Zieba JK, Calcutt MW, Foegeding NJ, Kim D, Kim J, Ryu S, Byndloss MX. Salmonella enterica serovar Typhimurium uses anaerobic respiration to overcome propionate-mediated colonization resistance. Cell Rep. 2022 Jan 1/4/2022; 38(1): 110180. PMID: 34986344, PMCID: PMC8800556, PII: S2211-1247(21)01680-6, DOI: 10.1016/j.celrep.2021.110180, ISSN: 2211-1247.

Peek CT, Ford CA, Eichelberger KR, Jacobse J, Torres TP, Maseda D, Latour YL, Piazuelo MB, Johnson JR, Byndloss MX, Wilson KT, Rathmell JC, Goettel JA, Cassat JE. Intestinal Inflammation Promotes MDL-1+ Osteoclast Precursor Expansion to Trigger Osteoclastogenesis and Bone Loss. Cell Mol Gastroenterol Hepatol [print-electronic]. 2022; 14(4): 731-50. PMID: 35835390, PMCID: PMC9420375, PII: S2352-345X(22)00160-6, DOI: 10.1016/j.jcmgh.2022.07.002, ISSN: 2352-345X.

Shealy NG, Yoo W, Byndloss MX. Colonization resistance: metabolic warfare as a strategy against pathogenic Enterobacteriaceae. Curr Opin Microbiol [print-electronic]. 2021 Dec; 64: 82-90. PMID: 34688039, PMCID: PMC8612973, PII: S1369-5274(21)00133-8, DOI: 10.1016/j.mib.2021.09.014, ISSN: 1879-0364.

Shealy NG, Byndloss MX. Trick and no treat: Carbohydrate preemption by commensal Enterobacteriaceae. Cell Host Microbe. 2021 Nov 11/10/2021; 29(11): 1606-8. PMID: 34762826, PII: S1931-3128(21)00470-4, DOI: 10.1016/j.chom.2021.10.006, ISSN: 1934-6069.

Yoo W, Zieba JK, Foegeding NJ, Torres TP, Shelton CD, Shealy NG, Byndloss AJ, Cevallos SA, Gertz E, Tiffany CR, Thomas JD, Litvak Y, Nguyen H, Olsan EE, Bennett BJ, Rathmell JC, Major AS, Bäumler AJ, Byndloss MX. High-fat diet-induced colonocyte dysfunction escalates microbiota-derived trimethylamine N-oxide. Science. 2021 Aug 8/13/2021; 373(6556): 813-8. PMID: 34385401, PMCID: PMC8506909, PII: 373/6556/813, DOI: 10.1126/science.aba3683, ISSN: 1095-9203.

Shuler H, Cazares V, Marshall A, Garza-Lopez E, Hultman R, Francis TK, Rolle T, Byndloss MX, Starbird CA, Hicsasmaz I, AshShareef S, Neikirk K, Johnson PEC, Vue Z, Beasley HK, Williams A, Hinton A. Intentional mentoring: maximizing the impact of underrepresented future scientists in the 21st century. Pathog Dis. 2021 Jul 7/28/2021; 79(6): PMID: 34283236, PMCID: PMC8326955, PII: 6324567, DOI: 10.1093/femspd/ftab038, ISSN: 2049-632X.

Foegeding NJ, Byndloss MX. TAKing on cancer. Cell Host Microbe. 2021 Jun 6/9/2021; 29(6): 851-3. PMID: 34111391, PII: S1931-3128(21)00233-X, DOI: 10.1016/j.chom.2021.05.005, ISSN: 1934-6069.

Yoo W, Choi J, Park B, Byndloss MX, Ryu S. A Nitrogen Metabolic Enzyme Provides Salmonella Fitness Advantage by Promoting Utilization of Microbiota-Derived Carbon Source. ACS Infect Dis [print-electronic]. 2021 May 5/14/2021; 7(5): 1208-20. PMID: 33853321, PMCID: PMC8603301, DOI: 10.1021/acsinfecdis.0c00836, ISSN: 2373-8227.

Foegeding NJ, Jones ZS, Byndloss MX. Western lifestyle as a driver of dysbiosis in colorectal cancer. Dis Model Mech [print-electronic]. 2021 May 5/1/2021; 14(5): PMID: 34060626, PMCID: PMC8214737, PII: 268972, DOI: 10.1242/dmm.049051, ISSN: 1754-8411.

Cevallos SA, Lee JY, Velazquez EM, Foegeding NJ, Shelton CD, Tiffany CR, Parry BH, Stull-Lane AR, Olsan EE, Savage HP, Nguyen H, Ghanaat SS, Byndloss AJ, Agu IO, Tsolis RM, Byndloss MX, Bäumler AJ. 5-Aminosalicylic Acid Ameliorates Colitis and Checks Dysbiotic Escherichia coli Expansion by Activating PPAR-¿ Signaling in the Intestinal Epithelium. MBio. 2021 Jan 1/19/2021; 12(1): PMID: 33468700, PMCID: PMC7845635, PII: mBio.03227-20, DOI: 10.1128/mBio.03227-20, ISSN: 2150-7511.

Lee JY, Cevallos SA, Byndloss MX, Tiffany CR, Olsan EE, Butler BP, Young BM, Rogers AWL, Nguyen H, Kim K, Choi SW, Bae E, Lee JH, Min UG, Lee DC, Bäumler AJ. High-Fat Diet and Antibiotics Cooperatively Impair Mitochondrial Bioenergetics to Trigger Dysbiosis that Exacerbates Pre-inflammatory Bowel Disease. Cell Host Microbe [print-electronic]. 2020 Aug 8/12/2020; 28(2): 273-284.e6-284.e6. PMID: 32668218, PMCID: PMC7429289, PII: S1931-3128(20)30303-6, DOI: 10.1016/j.chom.2020.06.001, ISSN: 1934-6069.

Byndloss MX. Microbial management. Science. 2020 Jul 7/10/2020; 369(6500): 153. PMID: 32646994, PII: 369/6500/153-a, DOI: 10.1126/science.abc5619, ISSN: 1095-9203.

Pham OH, Lee B, Labuda J, Keestra-Gounder AM, Byndloss MX, Tsolis RM, McSorley SJ. NOD1/NOD2 and RIP2 Regulate Endoplasmic Reticulum Stress-Induced Inflammation during Chlamydia Infection. MBio. 2020 Jun 6/2/2020; 11(3): PMID: 32487756, PMCID: PMC7267884, PII: mBio.00979-20, DOI: 10.1128/mBio.00979-20, ISSN: 2150-7511.

Shelton CD, Byndloss MX. Gut epithelial metabolism as a key driver of intestinal dysbiosis associated with noncommunicable diseases. Infect. Immun [print-electronic]. 2020 Mar 3/2/2020; PMID: 32122941, PII: IAI.00939-19, DOI: 10.1128/IAI.00939-19, ISSN: 1098-5522.

Yoo W, Byndloss MX. How to thrive in the inflamed gut. Nat Microbiol. 2020 Jan; 5(1): 10-1. PMID: 31857729, PII: 10.1038/s41564-019-0642-z, DOI: 10.1038/s41564-019-0642-z, ISSN: 2058-5276.

Pusceddu MM, Barboza M, Keogh CE, Schneider M, Stokes P, Sladek JA, Jung Danielle Kim H, Torres-Fuentes C, Goldfild LR, Gillis SE, Brust-Mascher I, Rabasa G, Wong KA, Lebrilla C, Byndloss MX, Maisonneuve C, Bäumler AJ, Philpott DJ, Ferrero RL, Barrett KE, Reardon C, Gareau MG. Nod-like receptors are critical for gut-brain axis signalling in mice. J. Physiol. (Lond.) [print-electronic]. 2019 Oct 10/25/2019; PMID: 31652348, DOI: 10.1113/JP278640, ISSN: 1469-7793.

Zhu W, Miyata N, Winter MG, Arenales A, Hughes ER, Spiga L, Kim J, Sifuentes-Dominguez L, Starokadomskyy P, Gopal P, Byndloss MX, Santos RL, Burstein E, Winter SE. Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer. J. Exp. Med [print-electronic]. 2019 Oct 10/7/2019; 216(10): 2378-93. PMID: 31358565, PMCID: PMC6781011, PII: jem.20181939, DOI: 10.1084/jem.20181939, ISSN: 1540-9538.

Cevallos SA, Lee JY, Tiffany CR, Byndloss AJ, Johnston L, Byndloss MX, Bäumler AJ. Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria. MBio. 2019 Oct 10/1/2019; 10(5): PMID: 31575772, PMCID: PMC6775460, PII: mBio.02244-19, DOI: 10.1128/mBio.02244-19, ISSN: 2150-7511.

Byndloss MX, Tsai AY, Walker GT, Miller CN, Young BM, English BC, Seyffert N, Kerrinnes T, de Jong MF, Atluri VL, Winter MG, Celli J, Tsolis RM. Brucella abortus Infection of Placental Trophoblasts Triggers Endoplasmic Reticulum Stress-Mediated Cell Death and Fetal Loss via Type IV Secretion System-Dependent Activation of CHOP. MBio. 2019 Jul 7/23/2019; 10(4): PMID: 31337727, PMCID: PMC6650558, PII: mBio.01538-19, DOI: 10.1128/mBio.01538-19, ISSN: 2150-7511.

Yum LK, Byndloss MX, Feldman SH, Agaisse H. Critical role of bacterial dissemination in an infant rabbit model of bacillary dysentery. Nat Commun. 2019 Apr 4/23/2019; 10(1): 1826. PMID: 31015451, PMCID: PMC6478941, PII: 10.1038/s41467-019-09808-4, DOI: 10.1038/s41467-019-09808-4, ISSN: 2041-1723.

Byndloss MX, Litvak Y, Bäumler AJ. Microbiota-nourishing Immunity and Its Relevance for Ulcerative Colitis. Inflamm Bowel Dis. 2019 Apr 4/11/2019; 25(5): 811-5. PMID: 30698700, PMCID: PMC6769399, PII: 5304210, DOI: 10.1093/ibd/izz004, ISSN: 1536-4844.

Velazquez EM, Nguyen H, Heasley KT, Saechao CH, Gil LM, Rogers AWL, Miller BM, Rolston MR, Lopez CA, Litvak Y, Liou MJ, Faber F, Bronner DN, Tiffany CR, Byndloss MX, Byndloss AJ, Bäumler AJ. Endogenous Enterobacteriaceae underlie variation in susceptibility to Salmonella infection. Nat Microbiol [print-electronic]. 2019 Mar 3/25/2019; PMID: 30911125, PII: 10.1038/s41564-019-0407-8, DOI: 10.1038/s41564-019-0407-8, ISSN: 2058-5276.

Byndloss MX, Litvak Y, Bäumler AJ. Microbiota-nourishing Immunity and Its Relevance for Ulcerative Colitis. Inflamm. Bowel Dis [print-electronic]. 2019 Jan 1/30/2019; PMID: 30698700, PII: 5304210, DOI: 10.1093/ibd/izz004, ISSN: 1536-4844.

Litvak Y, Mon KKZ, Nguyen H, Chanthavixay G, Liou M, Velazquez EM, Kutter L, Alcantara MA, Byndloss MX, Tiffany CR, Walker GT, Faber F, Zhu Y, Bronner DN, Byndloss AJ, Tsolis RM, Zhou H, Bäumler AJ. Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition. Cell Host Microbe. 2019 Jan 1/9/2019; 25(1): 128-139.e5. PMID: 30629913, PII: S1931-3128(18)30630-9, DOI: 10.1016/j.chom.2018.12.003, ISSN: 1934-6069.

Litvak Y, Byndloss MX, Bäumler AJ. Colonocyte metabolism shapes the gut microbiota. Science. 2018 Nov 11/30/2018; 362(6418): PMID: 30498100, PII: 362/6418/eaat9076, DOI: 10.1126/science.aat9076, ISSN: 1095-9203.

Byndloss MX, Pernitzsch SR, Bäumler AJ. Healthy hosts rule within: ecological forces shaping the gut microbiota. Mucosal Immunol [print-electronic]. 2018 May 5/9/2018; PMID: 29743614, PII: 10.1038/s41385-018-0010-y, DOI: 10.1038/s41385-018-0010-y, ISSN: 1935-3456.

Bronner DN, Faber F, Olsan EE, Byndloss MX, Sayed NA, Xu G, Yoo W, Kim D, Ryu S, Lebrilla CB, Bäumler AJ. Genetic Ablation of Butyrate Utilization Attenuates Gastrointestinal Salmonella Disease. Cell Host Microbe. 2018 Feb 2/14/2018; 23(2): 266-273.e4. PMID: 29447698, PII: S1931-3128(18)30039-8, DOI: 10.1016/j.chom.2018.01.004, ISSN: 1934-6069.

Byndloss MX, Bäumler AJ. The germ-organ theory of non-communicable diseases. Nat. Rev. Microbiol [print-electronic]. 2018 Feb; 16(2): 103-10. PMID: 29307890, PII: nrmicro.2017.158, DOI: 10.1038/nrmicro.2017.158, ISSN: 1740-1534.

Zhu W, Winter MG, Byndloss MX, Spiga L, Duerkop BA, Hughes ER, Büttner L, de Lima Romão E, Behrendt CL, Lopez CA, Sifuentes-Dominguez L, Huff-Hardy K, Wilson RP, Gillis CC, Tükel Ç, Koh AY, Burstein E, Hooper LV, Bäumler AJ, Winter SE. Precision editing of the gut microbiota ameliorates colitis. Nature [print-electronic]. 2018 Jan 1/11/2018; 553(7687): 208-11. PMID: 29323293, PMCID: PMC5804340, PII: nature25172, DOI: 10.1038/nature25172, ISSN: 1476-4687.

Frönicke L, Bronner DN, Byndloss MX, McLaughlin B, Bäumler AJ, Westermann AJ. Toward Cell Type-Specific In Vivo Dual RNA-Seq. Meth. Enzymol [print-electronic]. 2018; 612: 505-22. PMID: 30502956, PII: S0076-6879(18)30291-X, DOI: 10.1016/bs.mie.2018.08.013, ISSN: 1557-7988.

Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr. Opin. Microbiol [print-electronic]. 2017 Oct; 39: 1-6. PMID: 28783509, PII: S1369-5274(16)30220-X, DOI: 10.1016/j.mib.2017.07.003, ISSN: 1879-0364.

Byndloss MX, Olsan EE, Rivera-Chávez F, Tiffany CR, Cevallos SA, Lokken KL, Torres TP, Byndloss AJ, Faber F, Gao Y, Litvak Y, Lopez CA, Xu G, Napoli E, Giulivi C, Tsolis RM, Revzin A, Lebrilla CB, Bäumler AJ. Microbiota-activated PPAR-¿ signaling inhibits dysbiotic Enterobacteriaceae expansion. Science. 2017 Aug 8/11/2017; 357(6351): 570-5. PMID: 28798125, PMCID: PMC5642957, PII: 357/6351/570, DOI: 10.1126/science.aam9949, ISSN: 1095-9203.

Olsan EE, Byndloss MX, Faber F, Rivera-Chávez F, Tsolis RM, Bäumler AJ. Colonization resistance: The deconvolution of a complex trait. J. Biol. Chem [print-electronic]. 2017 May 5/26/2017; 292(21): 8577-81. PMID: 28389556, PMCID: PMC5448087, PII: R116.752295, DOI: 10.1074/jbc.R116.752295, ISSN: 1083-351X.

Byndloss MX, Rivera-Chávez F, Tsolis RM, Bäumler AJ. How bacterial pathogens use type III and type IV secretion systems to facilitate their transmission. Curr. Opin. Microbiol [print-electronic]. 2017 Feb; 35: 1-7. PMID: 27621139, PII: S1369-5274(16)30124-2, DOI: 10.1016/j.mib.2016.08.007, ISSN: 1879-0364.

Faber F, Thiennimitr P, Spiga L, Byndloss MX, Litvak Y, Lawhon S, Andrews-Polymenis HL, Winter SE, Bäumler AJ. Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis. PLoS Pathog. 2017 Jan; 13(1): e1006129. PMID: 28056091, PMCID: PMC5215881, PII: PPATHOGENS-D-16-01914, DOI: 10.1371/journal.ppat.1006129, ISSN: 1553-7374.

Costa LF, Mol JP, Silva AP, Macêdo AA, Silva TM, Alves GE, Winter S, Winter MG, Velazquez EM, Byndloss MX, Bäumler AJ, Tsolis RM, Paixão TA, Santos RL. Iron acquisition pathways and colonization of the inflamed intestine by Salmonella enterica serovar Typhimurium. Int. J. Med. Microbiol [print-electronic]. 2016 Dec; 306(8): 604-10. PMID: 27760693, PMCID: PMC5140723, PII: S1438-4221(16)30312-5, DOI: 10.1016/j.ijmm.2016.10.004, ISSN: 1618-0607.

Lopez CA, Miller BM, Rivera-Chávez F, Velazquez EM, Byndloss MX, Chávez-Arroyo A, Lokken KL, Tsolis RM, Winter SE, Bäumler AJ. Virulence factors enhance Citrobacter rodentium expansion through aerobic respiration. Science [print-electronic]. 2016 Sep 9/16/2016; 353(6305): 1249-53. PMID: 27634526, PMCID: PMC5127919, PII: 353/6305/1249, DOI: 10.1126/science.aag3042, ISSN: 1095-9203.

Byndloss MX, Keestra-Gounder AM, Bäumler AJ, Tsolis RM. NOD1 and NOD2: New Functions Linking Endoplasmic Reticulum Stress and Inflammation. DNA Cell Biol [print-electronic]. 2016 Jul; 35(7): 311-3. PMID: 27341284, PMCID: PMC4939383, DOI: 10.1089/dna.2016.3396, ISSN: 1557-7430.

Faber F, Tran L, Byndloss MX, Lopez CA, Velazquez EM, Kerrinnes T, Nuccio SP, Wangdi T, Fiehn O, Tsolis RM, Bäumler AJ. Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion. Nature [print-electronic]. 2016 Jun 6/30/2016; 534(7609): 697-9. PMID: 27309805, PMCID: PMC4939260, PII: nature18597, DOI: 10.1038/nature18597, ISSN: 1476-4687.

Keestra-Gounder AM, Byndloss MX, Seyffert N, Young BM, Chávez-Arroyo A, Tsai AY, Cevallos SA, Winter MG, Pham OH, Tiffany CR, de Jong MF, Kerrinnes T, Ravindran R, Luciw PA, McSorley SJ, Bäumler AJ, Tsolis RM. NOD1 and NOD2 signalling links ER stress with inflammation. Nature [print-electronic]. 2016 Apr 4/21/2016; 532(7599): 394-7. PMID: 27007849, PMCID: PMC4869892, PII: nature17631, DOI: 10.1038/nature17631, ISSN: 1476-4687.

Rivera-Chávez F, Zhang LF, Faber F, Lopez CA, Byndloss MX, Olsan EE, Xu G, Velazquez EM, Lebrilla CB, Winter SE, Bäumler AJ. Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella. Cell Host Microbe. 2016 Apr 4/13/2016; 19(4): 443-54. PMID: 27078066, PMCID: PMC4832419, PII: S1931-3128(16)30096-8, DOI: 10.1016/j.chom.2016.03.004, ISSN: 1934-6069.

Byndloss MX, Tsolis RM. Chronic Bacterial Pathogens: Mechanisms of Persistence. Microbiol Spectr. 2016 Apr; 4(2): PMID: 27227304, PMCID: PMC4888878, DOI: 10.1128/microbiolspec.VMBF-0020-2015, ISSN: 2165-0497.

Singletary LA, Karlinsey JE, Libby SJ, Mooney JP, Lokken KL, Tsolis RM, Byndloss MX, Hirao LA, Gaulke CA, Crawford RW, Dandekar S, Kingsley RA, Msefula CL, Heyderman RS, Fang FC. Loss of Multicellular Behavior in Epidemic African Nontyphoidal Salmonella enterica Serovar Typhimurium ST313 Strain D23580. MBio. 2016 Mar 3/1/2016; 7(2): e02265. PMID: 26933058, PMCID: PMC4810497, PII: mBio.02265-15, DOI: 10.1128/mBio.02265-15, ISSN: 2150-7511.

Byndloss MX, Tsolis RM. Brucella spp. Virulence Factors and Immunity. Annu Rev Anim Biosci [print-electronic]. 2016; 4: 111-27. PMID: 26734887, DOI: 10.1146/annurev-animal-021815-111326, ISSN: 2165-8110.

Mooney JP, Lokken KL, Byndloss MX, George MD, Velazquez EM, Faber F, Butler BP, Walker GT, Ali MM, Potts R, Tiffany C, Ahmer BM, Luckhart S, Tsolis RM. Inflammation-associated alterations to the intestinal microbiota reduce colonization resistance against non-typhoidal Salmonella during concurrent malaria parasite infection. Sci Rep. 2015 Oct 10/5/2015; 5: 14603. PMID: 26434367, PMCID: PMC4592952, PII: srep14603, DOI: 10.1038/srep14603, ISSN: 2045-2322.

Lopez CA, Rivera-Chávez F, Byndloss MX, Bäumler AJ. The Periplasmic Nitrate Reductase NapABC Supports Luminal Growth of Salmonella enterica Serovar Typhimurium during Colitis. Infect. Immun [print-electronic]. 2015 Sep; 83(9): 3470-8. PMID: 26099579, PMCID: PMC4534643, PII: IAI.00351-15, DOI: 10.1128/IAI.00351-15, ISSN: 1098-5522.

Mooney JP, Butler BP, Lokken KL, Xavier MN, Chau JY, Schaltenberg N, Dandekar S, George MD, Santos RL, Luckhart S, Tsolis RM. The mucosal inflammatory response to non-typhoidal Salmonella in the intestine is blunted by IL-10 during concurrent malaria parasite infection. Mucosal Immunol [print-electronic]. 2014 Nov; 7(6): 1302-11. PMID: 24670425, PMCID: PMC4177018, PII: mi201418, DOI: 10.1038/mi.2014.18, ISSN: 1935-3456.

Lokken KL, Mooney JP, Butler BP, Xavier MN, Chau JY, Schaltenberg N, Begum RH, Müller W, Luckhart S, Tsolis RM. Malaria parasite infection compromises control of concurrent systemic non-typhoidal Salmonella infection via IL-10-mediated alteration of myeloid cell function. PLoS Pathog. 2014 May; 10(5): e1004049. PMID: 24787713, PMCID: PMC4006898, PII: PPATHOGENS-D-13-02297, DOI: 10.1371/journal.ppat.1004049, ISSN: 1553-7374.

Spees AM, Kingsbury DD, Wangdi T, Xavier MN, Tsolis RM, Bäumler AJ. Neutrophils are a source of gamma interferon during acute Salmonella enterica serovar Typhimurium colitis. Infect. Immun [print-electronic]. 2014 Apr; 82(4): 1692-7. PMID: 24421037, PMCID: PMC3993401, PII: IAI.01508-13, DOI: 10.1128/IAI.01508-13, ISSN: 1098-5522.

Silva TM, Mol JP, Winter MG, Atluri V, Xavier MN, Pires SF, Paixão TA, Andrade HM, Santos RL, Tsolis RM. The predicted ABC transporter AbcEDCBA is required for type IV secretion system expression and lysosomal evasion by Brucella ovis. PLoS ONE. 2014; 9(12): e114532. PMID: 25474545, PMCID: PMC4256435, PII: PONE-D-14-28265, DOI: 10.1371/journal.pone.0114532, ISSN: 1932-6203.

Xavier MN, Winter MG, Spees AM, den Hartigh AB, Nguyen K, Roux CM, Silva TM, Atluri VL, Kerrinnes T, Keestra AM, Monack DM, Luciw PA, Eigenheer RA, Bäumler AJ, Santos RL, Tsolis RM. PPAR¿-mediated increase in glucose availability sustains chronic Brucella abortus infection in alternatively activated macrophages. Cell Host Microbe. 2013 Aug 8/14/2013; 14(2): 159-70. PMID: 23954155, PMCID: PMC3777723, PII: S1931-3128(13)00257-6, DOI: 10.1016/j.chom.2013.07.009, ISSN: 1934-6069.

Crawford RW, Wangdi T, Spees AM, Xavier MN, Tsolis RM, Bäumler AJ. Loss of very-long O-antigen chains optimizes capsule-mediated immune evasion by Salmonella enterica serovar Typhi. MBio. 2013 Jul 7/16/2013; 4(4): PMID: 23860765, PMCID: PMC3735119, PII: mBio.00232-13, DOI: 10.1128/mBio.00232-13, ISSN: 2150-7511.

Spees AM, Wangdi T, Lopez CA, Kingsbury DD, Xavier MN, Winter SE, Tsolis RM, Bäumler AJ. Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. MBio. 2013 Jul 7/2/2013; 4(4): PMID: 23820397, PMCID: PMC3705454, PII: mBio.00430-13, DOI: 10.1128/mBio.00430-13, ISSN: 2150-7511.

Terwagne M, Ferooz J, Rolán HG, Sun YH, Atluri V, Xavier MN, Franchi L, Núñez G, Legrand T, Flavell RA, De Bolle X, Letesson JJ, Tsolis RM. Innate immune recognition of flagellin limits systemic persistence of Brucella. Cell. Microbiol [print-electronic]. 2013 Jun; 15(6): 942-60. PMID: 23227931, PMCID: PMC4026035, DOI: 10.1111/cmi.12088, ISSN: 1462-5822.

Keestra AM, Winter MG, Auburger JJ, Frässle SP, Xavier MN, Winter SE, Kim A, Poon V, Ravesloot MM, Waldenmaier JF, Tsolis RM, Eigenheer RA, Bäumler AJ. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature [print-electronic]. 2013 Apr 4/11/2013; 496(7444): 233-7. PMID: 23542589, PMCID: PMC3625479, PII: nature12025, DOI: 10.1038/nature12025, ISSN: 1476-4687.

Moustacas VS, Silva TM, Costa LF, Xavier MN, Carvalho CA, Costa ÉA, Paixão TA, Santos RL. Species-specific multiplex PCR for the diagnosis of Brucella ovis, Actinobacillus seminis, and Histophilus somni infection in rams. BMC Vet. Res. 2013 Mar 3/21/2013; 9: 51. PMID: 23514236, PMCID: PMC3614447, PII: 1746-6148-9-51, DOI: 10.1186/1746-6148-9-51, ISSN: 1746-6148.

Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, Laughlin RC, Gomez G, Wu J, Lawhon SD, Popova IE, Parikh SJ, Adams LG, Tsolis RM, Stewart VJ, Bäumler AJ. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. 2013 Feb 2/8/2013; 339(6120): 708-11. PMID: 23393266, PMCID: PMC4004111, PII: 339/6120/708, DOI: 10.1126/science.1232467, ISSN: 1095-9203.

Xavier MN, Winter MG, Spees AM, Nguyen K, Atluri VL, Silva TM, Bäumler AJ, Müller W, Santos RL, Tsolis RM. CD4+ T cell-derived IL-10 promotes Brucella abortus persistence via modulation of macrophage function. PLoS Pathog [print-electronic]. 2013; 9(6): e1003454. PMID: 23818855, PMCID: PMC3688575, PII: PPATHOGENS-D-13-00074, DOI: 10.1371/journal.ppat.1003454, ISSN: 1553-7374.

Rivera-Chávez F, Winter SE, Lopez CA, Xavier MN, Winter MG, Nuccio SP, Russell JM, Laughlin RC, Lawhon SD, Sterzenbach T, Bevins CL, Tsolis RM, Harshey R, Adams LG, Bäumler AJ. Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog [print-electronic]. 2013; 9(4): e1003267. PMID: 23637594, PMCID: PMC3630101, PII: PPATHOGENS-D-12-02005, DOI: 10.1371/journal.ppat.1003267, ISSN: 1553-7374.

Crawford RW, Keestra AM, Winter SE, Xavier MN, Tsolis RM, Tolstikov V, Bäumler AJ. Very long O-antigen chains enhance fitness during Salmonella-induced colitis by increasing bile resistance. PLoS Pathog [print-electronic]. 2012 Sep; 8(9): e1002918. PMID: 23028318, PMCID: PMC3447750, PII: PPATHOGENS-D-12-00920, DOI: 10.1371/journal.ppat.1002918, ISSN: 1553-7374.

Lopez CA, Winter SE, Rivera-Chávez F, Xavier MN, Poon V, Nuccio SP, Tsolis RM, Bäumler AJ. Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration. MBio [electronic-print]. 2012; 3(3): PMID: 22691391, PMCID: PMC3374392, PII: mBio.00143-12, DOI: 10.1128/mBio.00143-12, ISSN: 2150-7511.

Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. U.S.A [print-electronic]. 2011 Oct 10/18/2011; 108(42): 17480-5. PMID: 21969563, PMCID: PMC3198331, PII: 1107857108, DOI: 10.1073/pnas.1107857108, ISSN: 1091-6490.

Santos RL, Almeida AP, Xavier MN, Paixão TA, Wilson RP, Dandekar S, Raffatellu M, Bäumler AJ. Enteric pathology and Salmonella-induced cell death in healthy and SIV-infected rhesus macaques. Vet. Pathol [print-electronic]. 2011 Sep; 48(5): 933-41. PMID: 21041540, PII: 0300985810386468, DOI: 10.1177/0300985810386468, ISSN: 1544-2217.

Keestra AM, Godinez I, Xavier MN, Winter MG, Winter SE, Tsolis RM, Bäumler AJ. Early MyD88-dependent induction of interleukin-17A expression during Salmonella colitis. Infect. Immun [print-electronic]. 2011 Aug; 79(8): 3131-40. PMID: 21576324, PMCID: PMC3147556, PII: IAI.00018-11, DOI: 10.1128/IAI.00018-11, ISSN: 1098-5522.

Tsolis RM, Xavier MN, Santos RL, Bäumler AJ. How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect. Immun [print-electronic]. 2011 May; 79(5): 1806-14. PMID: 21343352, PMCID: PMC3088149, PII: IAI.01369-10, DOI: 10.1128/IAI.01369-10, ISSN: 1098-5522.

Silva TM, Paixão TA, Costa EA, Xavier MN, Sá JC, Moustacas VS, den Hartigh AB, Carvalho Neta AV, Oliveira SC, Tsolis R, Santos RL. Putative ATP-binding cassette transporter is essential for Brucella ovis pathogenesis in mice. Infect. Immun [print-electronic]. 2011 Apr; 79(4): 1706-17. PMID: 21300772, PMCID: PMC3067543, PII: IAI.01109-10, DOI: 10.1128/IAI.01109-10, ISSN: 1098-5522.

Keestra AM, Winter MG, Klein-Douwel D, Xavier MN, Winter SE, Kim A, Tsolis RM, Bäumler AJ. A Salmonella virulence factor activates the NOD1/NOD2 signaling pathway. MBio [electronic-print]. 2011; 2(6): PMID: 22186610, PMCID: PMC3238304, PII: mBio.00266-11, DOI: 10.1128/mBio.00266-11, ISSN: 2150-7511.

Atluri VL, Xavier MN, de Jong MF, den Hartigh AB, Tsolis RM. Interactions of the human pathogenic Brucella species with their hosts. Annu. Rev. Microbiol. 2011; 65: 523-41. PMID: 21939378, DOI: 10.1146/annurev-micro-090110-102905, ISSN: 1545-3251.

Moustacas VS, Xavier MN, Carvalho-Júnior CA, Costa EA, Henry M, Santos RL. Effect of extender supplementation with various antimicrobial agents on viability of Brucella ovis and Actinobacillus seminis in cryopreserved ovine semen. Theriogenology [print-electronic]. 2010 Nov; 74(8): 1476-81. PMID: 20708246, PII: S0093-691X(10)00337-7, DOI: 10.1016/j.theriogenology.2010.06.019, ISSN: 1879-3231.

Xavier MN, Silva TM, Costa EA, Paixão TA, Moustacas VS, Carvalho CA, Sant'Anna FM, Robles CA, Gouveia AM, Lage AP, Tsolis RM, Santos RL. Development and evaluation of a species-specific PCR assay for the detection of Brucella ovis infection in rams. Vet. Microbiol [print-electronic]. 2010 Sep 9/28/2010; 145(1-2): 158-64. PMID: 20347534, PII: S0378-1135(10)00132-X, DOI: 10.1016/j.vetmic.2010.02.037, ISSN: 1873-2542.

Carvalho Neta AV, Mol JP, Xavier MN, Paixão TA, Lage AP, Santos RL. Pathogenesis of bovine brucellosis. Vet. J [print-electronic]. 2010 May; 184(2): 146-55. PMID: 19733101, PII: S1090-0233(09)00151-8, DOI: 10.1016/j.tvjl.2009.04.010, ISSN: 1532-2971.

Malta MC, Tinoco HP, Xavier MN, Vieira AL, Costa EA, Santos RL. Naturally acquired visceral leishmaniasis in non-human primates in Brazil. Vet. Parasitol [print-electronic]. 2010 Apr 4/19/2010; 169(1-2): 193-7. PMID: 20056328, PII: S0304-4017(09)00739-0, DOI: 10.1016/j.vetpar.2009.12.016, ISSN: 1873-2550.

Rolán HG, Xavier MN, Santos RL, Tsolis RM. Natural antibody contributes to host defense against an attenuated Brucella abortus virB mutant. Infect. Immun [print-electronic]. 2009 Jul; 77(7): 3004-13. PMID: 19364836, PMCID: PMC2708545, PII: IAI.01114-08, DOI: 10.1128/IAI.01114-08, ISSN: 1098-5522.

Silva FL, Oliveira RG, Silva TM, Xavier MN, Nascimento EF, Santos RL. Venereal transmission of canine visceral leishmaniasis. Vet. Parasitol [print-electronic]. 2009 Mar 3/9/2009; 160(1-2): 55-9. PMID: 19046812, PII: S0304-4017(08)00603-1, DOI: 10.1016/j.vetpar.2008.10.079, ISSN: 0304-4017.

Bueno R, Carvalho Neta AV, Xavier MN, Oliveira RG, Diniz SA, Melo MN, Santos RL. CDNA sequencing and expression of Nramp1 (Slc11a1) in dogs phenotypically resistant or susceptible to visceral leishmaniasis. Vet. Immunol. Immunopathol [print-electronic]. 2009 Feb 2/15/2009; 127(3-4): 332-9. PMID: 19084282, PII: S0165-2427(08)00722-8, DOI: 10.1016/j.vetimm.2008.10.335, ISSN: 0165-2427.

Xavier MN, Paixão TA, Poester FP, Lage AP, Santos RL. Pathological, immunohistochemical and bacteriological study of tissues and milk of cows and fetuses experimentally infected with Brucella abortus. J. Comp. Pathol [print-electronic]. 2009 Feb; 140(2-3): 149-57. PMID: 19111839, PII: S0021-9975(08)00141-2, DOI: 10.1016/j.jcpa.2008.10.004, ISSN: 1532-3129.

Silva FL, Rodrigues AA, Rego IO, Santos RL, Oliveira RG, Silva TM, Xavier MN, Nascimento EF, Santos RL. Genital lesions and distribution of amastigotes in bitches naturally infected with Leishmania chagasi. Vet. Parasitol [print-electronic]. 2008 Jan 1/25/2008; 151(1): 86-90. PMID: 18006233, PII: S0304-4017(07)00528-6, DOI: 10.1016/j.vetpar.2007.09.032, ISSN: 0304-4017.