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Howard A. Shuman

TitleProfessor
InstitutionUniversity of Chicago
DepartmentMicrobiology
AddressChicago IL 60637
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    Collapse Overview 
    Collapse overview
    Our group is interested in how intracellular bacterial pathogens interact with and commandeer host cell functions during infection. We have studied the intracellular human pathogen, Legionella pneumophila for more than 30 years. This gram-negative species causes an acute febrile pneumonia called Legionnaires’ disease. People become infected with Legionella when they inhale contaminated aerosols. This can happen when cooling and ventilation systems, fountains, or whirlpools become contaminated. In these environments, Legionella replicates in single-celled amoebae. In human lungs these bacteria can infect and replicate in alveolar macrophages.

    In order to understand how Legionella is able to survive and grow inside amoebae and macrophages, we use genetic and genomic approaches to ask which functions in the bacteria and which ones in the host are important for infection. We found that Legionella has a “Type IV Secretion System” called the Icm/Dot System that translocates protein “effectors” to the host cell and that these effectors dramatically alter organelle trafficking in host cells as is shown in the accompanying diagram. The Legionella – containing vacuole, (LCV) is where the bacteria grow within cells in a nutrient-rich, protected niche.

    Current Position:

    2010 - Professor of Microbiology, University of Chicago

    Education:

    1970-1974 University of Massachusetts, B.S. (Microbiology, honors)
    1975-1980 Harvard University, Ph.D. (Biological Chemistry)
    1980-1982 Postdoctoral Fellow, Department of Biochemistry & Molecular Biology, Harvard University

    Employment / Experience:

    1974-1975 Research Assistant, Institut Pasteur, Paris, France
    1982-1989 Assistant Professor, Department of Microbiology, Columbia University
    1989-1995 Associate Professor, Department of Microbiology, Columbia University
    1995- 2010 Professor, Department of Microbiology, Columbia University
    2005- 2008 Director of Graduate Studies, Department of Microbiology, Columbia University
    2008 Interim Chair, Department of Microbiology, Columbia University
    2010 Professor Emeritus, Department of Microbiology & Immunology, Columbia University
    2010-2015 Director, Howard Taylor Ricketts Regional Biocontainment Laboratory

    Professional Service:

    1986- 1997 Editorial Board, Journal of Bacteriology
    1989- 1992 Editorial Board, Infection and Immunity
    1994- 1999 Editorial Board, The Journal of Biological Chemistry
    1998 Co-Chair, Gordon Research Conference: "Bacterial Cell Surfaces"
    2007 Guest Editor, Proceedings of the National Academy of Sciences
    2009 Editorial Board, Protist
    2009 - 2010 Steering Committee, Northeast Biodefense Center
    2009 - 2019 Editorial Board, mBio

    Collapse Biography 
    Collapse education and training
    University of Massachusetts, Amherst, MAB.S.1974Microbiology
    Harvard University, Boston, MAPh.D.1980Biological Chemistry
    Collapse awards and honors
    1980 - 1982Fellow, Jane Coffin Childs Memorial Fund, Jane Coffin Childs Memorial Fund
    1983 - 1988Career Scientist, Irma T. Hirschl Charitable Trust, Irma T. Hirschl Charitable Trust
    1989 - 1994Faculty Research Awardee, American Cancer Societ, American Cancer Society
    1991 - 1996Max Planck Award (co-recipient), A. v. Humboldt Foundation/Max Planck Society, A. v. Humboldt Foundation/Max Planck Society
    2003Fellow, American Academy of Microbiology, American Academy of Microbiology
    2007Lady Davis Visiting Professor, Hebrew University, Hebrew University
    2009Fellow, American Association for the Advancement of Science, American Association for the Advancement of Science
    2010Karin Ippen-Ihler Memorial Lecturer, Texas A&M Medical School, Texas A&M Medical School

    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    Newest   |   Oldest   |   Most Cited   |   Most Discussed   |   Timeline   |   Field Summary   |   Plain Text
    PMC Citations indicate the number of times the publication was cited by articles in PubMed Central, and the Altmetric score represents citations in news articles and social media. (Note that publications are often cited in additional ways that are not shown here.) Fields are based on how the National Library of Medicine (NLM) classifies the publication's journal and might not represent the specific topic of the publication. Translation tags are based on the publication type and the MeSH terms NLM assigns to the publication. Some publications (especially newer ones and publications not in PubMed) might not yet be assigned Field or Translation tags.) Click a Field or Translation tag to filter the publications.
    1. Bisaro F, Shuman HA, Feldman MF, Gebhardt MJ, Pukatzki S. Acinetobacter baumannii ATCC 17978 encodes a microcin system with antimicrobial properties for contact-independent competition. Microbiology (Reading). 2023 06; 169(6). PMID: 37289493; PMCID: PMC10333792.
      Citations: 1     Fields:    Translation:HumansCells
    2. Zhou H, Gebhardt MJ, Czyz DM, Yao Y, Shuman HA. The gigA/gigB Genes Regulate the Growth, Stress Response, and Virulence of Acinetobacter baumannii ATCC 17978 Strain. Front Microbiol. 2021; 12:723949. PMID: 34421881; PMCID: PMC8371402.
      Citations: 3     
    3. Gebhardt MJ, Czyz DM, Singh S, Zurawski DV, Becker L, Shuman HA. GigC, a LysR Family Transcription Regulator, Is Required for Cysteine Metabolism and Virulence in Acinetobacter baumannii. Infect Immun. 2020 12 15; 89(1). PMID: 33077621; PMCID: PMC7927930.
      Citations: 9     Fields:    Translation:AnimalsCells
    4. Repizo GD, Seravalle JL, Shuman HA, Viale AM, Espariz M, Díaz Miloslavich JI, Steimbrüch BA. Acinetobacter baumannii NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms. mSphere. 2020 07 29; 5(4). PMID: 32727858; PMCID: PMC7392541.
      Citations: 7     Fields:    Translation:AnimalsCellsPHPublic Health
    5. Zhang D, Tang Z, Huang H, Zhou G, Cui C, Weng Y, Liu W, Kim S, Lee S, Perez-Neut M, Ding J, Czyz D, Hu R, Ye Z, He M, Zheng YG, Shuman HA, Dai L, Ren B, Roeder RG, Becker L, Zhao Y. Metabolic regulation of gene expression by histone lactylation. Nature. 2019 10; 574(7779):575-580. PMID: 31645732; PMCID: PMC6818755.
      Citations: 899     Fields:    Translation:HumansAnimalsCells
    6. Shuman H, Amaro F. Selection of Legionella Virulence-Related Traits by Environmental Protozoa. Methods Mol Biol. 2019; 1921:55-78. PMID: 30694485.
      Citations:    Fields:    Translation:AnimalsCellsPHPublic Health
    7. Goss CH, Kaneko Y, Khuu L, Anderson GD, Ravishankar S, Aitken ML, Lechtzin N, Zhou G, Czyz DM, McLean K, Olakanmi O, Shuman HA, Teresi M, Wilhelm E, Caldwell E, Salipante SJ, Hornick DB, Siehnel RJ, Becker L, Britigan BE, Singh PK. Gallium disrupts bacterial iron metabolism and has therapeutic effects in mice and humans with lung infections. Sci Transl Med. 2018 09 26; 10(460). PMID: 30257953; PMCID: PMC6637966.
      Citations: 96     Fields:    Translation:HumansAnimalsCellsCTClinical Trials
    8. Reardon CA, Lingaraju A, Schoenfelt KQ, Zhou G, Cui C, Jacobs-El H, Babenko I, Hoofnagle A, Czyz D, Shuman H, Vaisar T, Becker L. Obesity and Insulin Resistance Promote Atherosclerosis through an IFN?-Regulated Macrophage Protein Network. Cell Rep. 2018 06 05; 23(10):3021-3030. PMID: 29874587; PMCID: PMC6082182.
      Citations: 44     Fields:    Translation:AnimalsCells
    9. Gebhardt MJ, Shuman HA. GigA and GigB are Master Regulators of Antibiotic Resistance, Stress Responses, and Virulence in Acinetobacter baumannii. J Bacteriol. 2017 05 15; 199(10). PMID: 28264991; PMCID: PMC5405210.
      Citations: 21     Fields:    Translation:Cells
    10. Gebhardt MJ, Jacobson RK, Shuman HA. Seeing red; the development of pON.mCherry, a broad-host range constitutive expression plasmid for Gram-negative bacteria. PLoS One. 2017; 12(3):e0173116. PMID: 28257493; PMCID: PMC5336243.
      Citations: 6     Fields:    Translation:Cells
    11. Czyz DM, Jain-Gupta N, Shuman HA, Crosson S. A dual-targeting approach to inhibit Brucella abortus replication in human cells. Sci Rep. 2016 10 21; 6:35835. PMID: 27767061; PMCID: PMC5073326.
      Citations: 6     Fields:    Translation:HumansCells
    12. Shi X, Halder P, Yavuz H, Jahn R, Shuman HA. Direct targeting of membrane fusion by SNARE mimicry: Convergent evolution of Legionella effectors. Proc Natl Acad Sci U S A. 2016 08 02; 113(31):8807-12. PMID: 27436892; PMCID: PMC4978295.
      Citations: 20     Fields:    Translation:HumansCells
    13. Burstein D, Amaro F, Zusman T, Lifshitz Z, Cohen O, Gilbert JA, Pupko T, Shuman HA, Segal G. Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires. Nat Genet. 2016 Feb; 48(2):167-75. PMID: 26752266; PMCID: PMC5050043.
      Citations: 152     Fields:    Translation:Cells
    14. Gebhardt MJ, Gallagher LA, Jacobson RK, Usacheva EA, Peterson LR, Zurawski DV, Shuman HA. Joint Transcriptional Control of Virulence and Resistance to Antibiotic and Environmental Stress in Acinetobacter baumannii. mBio. 2015 Nov 10; 6(6):e01660-15. PMID: 26556274; PMCID: PMC4659468.
      Citations: 75     Fields:    Translation:AnimalsCells
    15. Amaro F, Wang W, Gilbert JA, Anderson OR, Shuman HA. Diverse protist grazers select for virulence-related traits in Legionella. ISME J. 2015 Jul; 9(7):1607-18. PMID: 25575308; PMCID: PMC4478701.
      Citations: 29     Fields:    Translation:HumansAnimalsCellsPHPublic Health
    16. Jacobs AC, Thompson MG, Gebhardt M, Corey BW, Yildirim S, Shuman HA, Zurawski DV. Genetic Manipulation of Acinetobacter baumannii. Curr Protoc Microbiol. 2014 Nov 03; 35:6G.2.1-11. PMID: 25367274.
      Citations: 15     Fields:    Translation:Cells
    17. Czyz DM, Potluri LP, Jain-Gupta N, Riley SP, Martinez JJ, Steck TL, Crosson S, Shuman HA, Gabay JE. Host-directed antimicrobial drugs with broad-spectrum efficacy against intracellular bacterial pathogens. mBio. 2014 Jul 29; 5(4):e01534-14. PMID: 25073644; PMCID: PMC4128363.
      Citations: 37     Fields:    Translation:HumansCells
    18. Lifshitz Z, Burstein D, Schwartz K, Shuman HA, Pupko T, Segal G. Identification of novel Coxiella burnetii Icm/Dot effectors and genetic analysis of their involvement in modulating a mitogen-activated protein kinase pathway. Infect Immun. 2014 Sep; 82(9):3740-52. PMID: 24958706; PMCID: PMC4187803.
      Citations: 41     Fields:    Translation:HumansAnimalsCells
    19. Trigui H, Dudyk P, Sum J, Shuman HA, Faucher SP. Analysis of the transcriptome of Legionella pneumophila hfq mutant reveals a new mobile genetic element. Microbiology (Reading). 2013 Aug; 159(Pt 8):1649-1660. PMID: 23728622; PMCID: PMC5972305.
      Citations: 8     Fields:    Translation:Cells
    20. Khweek AA, Caution K, Akhter A, Abdulrahman BA, Tazi M, Hassan H, Majumdar N, Doran A, Guirado E, Schlesinger LS, Shuman H, Amer AO. A bacterial protein promotes the recognition of the Legionella pneumophila vacuole by autophagy. Eur J Immunol. 2013 May; 43(5):1333-44. PMID: 23420491; PMCID: PMC3782291.
      Citations: 26     Fields:    Translation:HumansAnimalsCells
    21. Lu J, Struewing I, Buse HY, Kou J, Shuman HA, Ashbolt NJ, Faucher SP. Legionella pneumophila transcriptional response following exposure to CuO nanoparticles. Appl Environ Microbiol. 2013 Apr; 79(8):2713-20. PMID: 23416998; PMCID: PMC3623207.
      Citations: 12     Fields:    Translation:Cells
    22. Lifshitz Z, Burstein D, Peeri M, Zusman T, Schwartz K, Shuman HA, Pupko T, Segal G. Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal. Proc Natl Acad Sci U S A. 2013 Feb 19; 110(8):E707-15. PMID: 23382224; PMCID: PMC3581968.
      Citations: 103     Fields:    Translation:Cells
    23. Yu KO, Porcelli SA, Shuman HA. In vitro derivation of macrophage from guinea pig bone marrow with human M-CSF. J Immunol Methods. 2013 Mar 29; 389(1-2):88-94. PMID: 23333710.
      Citations:    Fields:    Translation:HumansAnimalsCells
    24. Faucher SP, Shuman HA. Methods to study legionella transcriptome in vitro and in vivo. Methods Mol Biol. 2013; 954:567-82. PMID: 23150421.
      Citations: 5     Fields:    Translation:Cells
    25. Amaro F, Gilbert JA, Owens S, Trimble W, Shuman HA. Whole-genome sequence of the human pathogen Legionella pneumophila serogroup 12 strain 570-CO-H. J Bacteriol. 2012 Mar; 194(6):1613-4. PMID: 22374950; PMCID: PMC3294838.
      Citations: 16     Fields:    Translation:HumansCells
    26. Franco IS, Shohdy N, Shuman HA. The Legionella pneumophila effector VipA is an actin nucleator that alters host cell organelle trafficking. PLoS Pathog. 2012 Feb; 8(2):e1002546. PMID: 22383880; PMCID: PMC3285593.
      Citations: 40     Fields:    Translation:HumansAnimalsCells
    27. Franco IS, Shuman HA. A pathogen's journey in the host cell: Bridges between actin and traffic. Bioarchitecture. 2012 Feb 01; 2(2):38-42. PMID: 22754628; PMCID: PMC3383720.
      Citations: 6     Fields:    
    28. Abdul-Sater AA, Grajkowski A, Erdjument-Bromage H, Plumlee C, Levi A, Schreiber MT, Lee C, Shuman H, Beaucage SL, Schindler C. The overlapping host responses to bacterial cyclic dinucleotides. Microbes Infect. 2012 Feb; 14(2):188-97. PMID: 21933720; PMCID: PMC3518029.
      Citations: 14     Fields:    Translation:HumansAnimalsCells
    29. Pronin SV, Martinez A, Kuznedelov K, Severinov K, Shuman HA, Kozmin SA. Chemical synthesis enables biochemical and antibacterial evaluation of streptolydigin antibiotics. J Am Chem Soc. 2011 Aug 10; 133(31):12172-84. PMID: 21714556; PMCID: PMC3174773.
      Citations: 12     Fields:    Translation:Cells
    30. Shuman HA, Faucher SP. Small Regulatory RNA and Legionella pneumophila. Front Microbiol. 2011; 2:98. PMID: 21833335; PMCID: PMC3153055.
      Citations: 15     
    31. Mueller CA, Shuman HA, Faucher SP. Legionella Pneumophila Transcriptome during Intracellular Multiplication in Human Macrophages. Front Microbiol. 2011; 2:60. PMID: 21747786; PMCID: PMC3128937.
      Citations: 59     
    32. Levi A, Folcher M, Jenal U, Shuman HA. Cyclic diguanylate signaling proteins control intracellular growth of Legionella pneumophila. mBio. 2011 Jan 11; 2(1):e00316-10. PMID: 21249170; PMCID: PMC3023162.
      Citations: 28     Fields:    Translation:HumansAnimalsCells
    33. Anderson OR, Wang W, Faucher SP, Bi K, Shuman HA. A new heterolobosean amoeba Solumitrus palustris n. g., n. sp. isolated from freshwater marsh soil. J Eukaryot Microbiol. 2011 Jan-Feb; 58(1):60-7. PMID: 21182560.
      Citations: 2     Fields:    Translation:Animals
    34. Charpentier X, Kay E, Schneider D, Shuman HA. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J Bacteriol. 2011 Mar; 193(5):1114-21. PMID: 21169481; PMCID: PMC3067580.
      Citations: 59     Fields:    Translation:HumansCells
    35. Hovel-Miner G, Faucher SP, Charpentier X, Shuman HA. ArgR-regulated genes are derepressed in the Legionella-containing vacuole. J Bacteriol. 2010 Sep; 192(17):4504-16. PMID: 20622069; PMCID: PMC2937375.
      Citations: 24     Fields:    Translation:HumansAnimalsCells
    36. Friedlander G, Livny J, Margalit H, Shuman HA, Faucher SP. Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci U S A. 2010 Apr 20; 107(16):7533-8. PMID: 20368425; PMCID: PMC2867745.
      Citations: 42     Fields:    Translation:Cells
    37. Paumet F, Wesolowski J, Garcia-Diaz A, Delevoye C, Aulner N, Shuman HA, Subtil A, Rothman JE. Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One. 2009 Oct 12; 4(10):e7375. PMID: 19823575; PMCID: PMC2756591.
      Citations: 51     Fields:    Translation:AnimalsCells
    38. Plumlee CR, Lee C, Beg AA, Decker T, Shuman HA, Schindler C. Interferons direct an effective innate response to Legionella pneumophila infection. J Biol Chem. 2009 Oct 30; 284(44):30058-66. PMID: 19720834; PMCID: PMC2781560.
      Citations: 49     Fields:    Translation:AnimalsCells
    39. Charpentier X, Reyes M, Zhu JW, Weiss A, Shuman HA, Gabay JE. Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog. 2009 Jul; 5(7):e1000501. PMID: 19578436; PMCID: PMC2698123.
      Citations: 54     Fields:    Translation:HumansAnimalsCells
    40. Franco IS, Shuman HA, Charpentier X. The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol. 2009 Oct; 11(10):1435-43. PMID: 19563462.
      Citations: 64     Fields:    Translation:HumansAnimalsCells
    41. Reich-Slotky R, Kabbash CA, Della-Latta P, Blanchard JS, Feinmark SJ, Freeman S, Kaplan G, Shuman HA, Silverstein SC. Gemfibrozil inhibits Legionella pneumophila and Mycobacterium tuberculosis enoyl coenzyme A reductases and blocks intracellular growth of these bacteria in macrophages. J Bacteriol. 2009 Aug; 191(16):5262-71. PMID: 19429621; PMCID: PMC2725597.
      Citations: 12     Fields:    Translation:HumansAnimalsCells
    42. Hovel-Miner G, Pampou S, Faucher SP, Clarke M, Morozova I, Morozov P, Russo JJ, Shuman HA, Kalachikov S. SigmaS controls multiple pathways associated with intracellular multiplication of Legionella pneumophila. J Bacteriol. 2009 Apr; 191(8):2461-73. PMID: 19218380; PMCID: PMC2668410.
      Citations: 58     Fields:    Translation:AnimalsCells
    43. Charpentier X, Kalachikov S, Shuman HA, Faucher SP. Loss of RNase R induces competence development in Legionella pneumophila. J Bacteriol. 2008 Dec; 190(24):8126-36. PMID: 18849432; PMCID: PMC2593228.
      Citations: 32     Fields:    Translation:Cells
    44. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, Pericone CD, Shuman HA. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 2008 Aug 01; 4(8):e1000117. PMID: 18670632; PMCID: PMC2475511.
      Citations: 154     Fields:    Translation:AnimalsCells
    45. Chen J, Reyes M, Clarke M, Shuman HA. Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell Microbiol. 2007 Jul; 9(7):1660-71. PMID: 17371403.
      Citations: 34     Fields:    Translation:HumansAnimalsCells
    46. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, Kalachikov S, Shuman HA. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol. 2005 Nov; 187(22):7716-26. PMID: 16267296; PMCID: PMC1280299.
      Citations: 151     Fields:    Translation:Cells
    47. Shohdy N, Efe JA, Emr SD, Shuman HA. Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci U S A. 2005 Mar 29; 102(13):4866-71. PMID: 15781869; PMCID: PMC555709.
      Citations: 105     Fields:    Translation:AnimalsCells
    48. Shuman HA, Albers U, Reus K, Hilbi H. The amoebae plate test implicates a paralogue of lpxB in the interaction of Legionella pneumophila with Acanthamoeba castellanii. Microbiology (Reading). 2005 Jan; 151(Pt 1):167-182. PMID: 15632436.
      Citations: 14     Fields:    Translation:HumansAnimalsCells
    49. Chien M, Morozova I, Shi S, Sheng H, Chen J, Gomez SM, Asamani G, Hill K, Nuara J, Feder M, Rineer J, Greenberg JJ, Steshenko V, Park SH, Zhao B, Teplitskaya E, Edwards JR, Pampou S, Georghiou A, Chou IC, Iannuccilli W, Ulz ME, Kim DH, Geringer-Sameth A, Goldsberry C, Morozov P, Fischer SG, Segal G, Qu X, Rzhetsky A, Zhang P, Cayanis E, De Jong PJ, Ju J, Kalachikov S, Shuman HA, Russo JJ. The genomic sequence of the accidental pathogen Legionella pneumophila. Science. 2004 Sep 24; 305(5692):1966-8. PMID: 15448271.
      Citations: 226     Fields:    Translation:Cells
    50. Morozova I, Qu X, Shi S, Asamani G, Greenberg JE, Shuman HA, Russo JJ. Comparative sequence analysis of the icm/dot genes in Legionella. Plasmid. 2004 Mar; 51(2):127-47. PMID: 15003709.
      Citations: 19     Fields:    Translation:Cells
    51. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, Segal G, Shuman HA. Legionella effectors that promote nonlytic release from protozoa. Science. 2004 Feb 27; 303(5662):1358-61. PMID: 14988561.
      Citations: 131     Fields:    Translation:HumansAnimalsCells
    52. Otto GP, Wu MY, Clarke M, Lu H, Anderson OR, Hilbi H, Shuman HA, Kessin RH. Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum. Mol Microbiol. 2004 Jan; 51(1):63-72. PMID: 14651611.
      Citations: 44     Fields:    Translation:AnimalsCells
    53. Miyamoto H, Yoshida S, Taniguchi H, Shuman HA. Virulence conversion of Legionella pneumophila by conjugal transfer of chromosomal DNA. J Bacteriol. 2003 Nov; 185(22):6712-8. PMID: 14594847; PMCID: PMC262088.
      Citations: 9     Fields:    Translation:HumansAnimalsCells
    54. Berry EA, Charvolin D, Creuzenet C, Ebel C, Engelman DM, Giusti F, Gohon Y, Hong Q, Lakey JH, Leonard K, Shuman HA, Timmins P, Warschawski DE, Zito F, Zoonens M, Pucci B, Tribet C, Popot JL, Flötenmeyer M. Amphipols: polymeric surfactants for membrane biology research. Cell Mol Life Sci. 2003 Aug; 60(8):1559-74. PMID: 14513831; PMCID: PMC11138540.
      Citations: 57     Fields:    Translation:AnimalsCells
    55. Samanta S, Ayvaz T, Reyes M, Shuman HA, Chen J, Davidson AL. Disulfide cross-linking reveals a site of stable interaction between C-terminal regulatory domains of the two MalK subunits in the maltose transport complex. J Biol Chem. 2003 Sep 12; 278(37):35265-71. PMID: 12813052.
      Citations: 17     Fields:    Translation:Cells
    56. Shuman HA, Silhavy TJ. The art and design of genetic screens: Escherichia coli. Nat Rev Genet. 2003 Jun; 4(6):419-31. PMID: 12776212.
      Citations: 40     Fields:    Translation:Cells
    57. Shuman HA. Just toothpicks and logic: how some labs succeed at solving complex problems. J Bacteriol. 2003 Jan; 185(2):387-90. PMID: 12511482; PMCID: PMC145328.
      Citations: 3     Fields:    Translation:Cells
    58. Steenbergen JN, Shuman HA, Casadevall A. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A. 2001 Dec 18; 98(26):15245-50. PMID: 11742090; PMCID: PMC65014.
      Citations: 228     Fields:    Translation:AnimalsCells
    59. Hilbi H, Segal G, Shuman HA. Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol. 2001 Nov; 42(3):603-17. PMID: 11722729.
      Citations: 70     Fields:    Translation:HumansAnimalsCells
    60. Khelef N, Shuman HA, Maxfield FR. Phagocytosis of wild-type Legionella pneumophila occurs through a wortmannin-insensitive pathway. Infect Immun. 2001 Aug; 69(8):5157-61. PMID: 11447198; PMCID: PMC98612.
      Citations: 19     Fields:    Translation:HumansCells
    61. Reich-Slotky R, Panagiotidis C, Reyes M, Shuman HA. The detergent-soluble maltose transporter is activated by maltose binding protein and verapamil. J Bacteriol. 2000 Feb; 182(4):993-1000. PMID: 10648525; PMCID: PMC94375.
      Citations: 12     Fields:    Translation:Cells
    62. Segal G, Russo JJ, Shuman HA. Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol Microbiol. 1999 Nov; 34(4):799-809. PMID: 10564519.
      Citations: 68     Fields:    Translation:HumansCells
    63. Hales LM, Shuman HA. The Legionella pneumophila rpoS gene is required for growth within Acanthamoeba castellanii. J Bacteriol. 1999 Aug; 181(16):4879-89. PMID: 10438758; PMCID: PMC93975.
      Citations: 79     Fields:    Translation:HumansAnimalsCells
    64. Segal G, Shuman HA. Possible origin of the Legionella pneumophila virulence genes and their relation to Coxiella burnetii. Mol Microbiol. 1999 Aug; 33(3):669-70. PMID: 10417657.
      Citations: 32     Fields:    Translation:HumansCells
    65. Hales LM, Shuman HA. Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun. 1999 Jul; 67(7):3662-6. PMID: 10377156; PMCID: PMC116561.
      Citations: 58     Fields:    Translation:AnimalsCells
    66. Segal G, Shuman HA. Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect Immun. 1999 May; 67(5):2117-24. PMID: 10225863; PMCID: PMC115946.
      Citations: 136     Fields:    Translation:HumansAnimalsCells
    67. Panagiotidis CH, Boos W, Shuman HA. The ATP-binding cassette subunit of the maltose transporter MalK antagonizes MalT, the activator of the Escherichia coli mal regulon. Mol Microbiol. 1998 Nov; 30(3):535-46. PMID: 9822819.
      Citations: 24     Fields:    Translation:Cells
    68. Segal G, Shuman HA. Intracellular multiplication and human macrophage killing by Legionella pneumophila are inhibited by conjugal components of IncQ plasmid RSF1010. Mol Microbiol. 1998 Oct; 30(1):197-208. PMID: 9786196.
      Citations: 54     Fields:    Translation:HumansCells
    69. Wiater LA, Dunn K, Maxfield FR, Shuman HA. Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect Immun. 1998 Sep; 66(9):4450-60. PMID: 9712800; PMCID: PMC108538.
      Citations: 53     Fields:    Translation:HumansCells
    70. Segal G, Shuman HA. How is the intracellular fate of the Legionella pneumophila phagosome determined? Trends Microbiol. 1998 Jul; 6(7):253-5. PMID: 9717210.
      Citations: 39     Fields:    Translation:Cells
    71. Purcell M, Shuman HA. The Legionella pneumophila icmGCDJBF genes are required for killing of human macrophages. Infect Immun. 1998 May; 66(5):2245-55. PMID: 9573114; PMCID: PMC108188.
      Citations: 44     Fields:    Translation:HumansCells
    72. Boos W, Shuman H. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev. 1998 Mar; 62(1):204-29. PMID: 9529892; PMCID: PMC98911.
      Citations: 241     Fields:    Translation:Cells
    73. Segal G, Purcell M, Shuman HA. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci U S A. 1998 Feb 17; 95(4):1669-74. PMID: 9465074; PMCID: PMC19142.
      Citations: 254     Fields:    Translation:HumansCells
    74. Merino G, Shuman HA. Truncation of MalF results in lactose transport via the maltose transport system of Escherichia coli. J Biol Chem. 1998 Jan 23; 273(4):2435-44. PMID: 9442094.
      Citations: 6     Fields:    Translation:Cells
    75. Panagiotidis CH, Shuman HA. Maltose transport in Escherichia coli: mutations that uncouple ATP hydrolysis from transport. Methods Enzymol. 1998; 292:30-9. PMID: 9711544.
      Citations: 3     Fields:    Translation:Cells
    76. Shuman HA, Purcell M, Segal G, Hales L, Wiater LA. Intracellular multiplication of Legionella pneumophila: human pathogen or accidental tourist? Curr Top Microbiol Immunol. 1998; 225:99-112. PMID: 9386330.
      Citations: 17     Fields:    Translation:HumansAnimalsCells
    77. Merino G, Shuman HA. Unliganded maltose-binding protein triggers lactose transport in an Escherichia coli mutant with an alteration in the maltose transport system. J Bacteriol. 1997 Dec; 179(24):7687-94. PMID: 9401026; PMCID: PMC179730.
      Citations: 12     Fields:    Translation:Cells
    78. Segal G, Shuman HA. Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect Immun. 1997 Dec; 65(12):5057-66. PMID: 9393796; PMCID: PMC175729.
      Citations: 69     Fields:    Translation:HumansCells
    79. al-Mehdi AB, Shuman H, Fisher AB. Oxidant generation with K(+)-induced depolarization in the isolated perfused lung. Free Radic Biol Med. 1997; 23(1):47-56. PMID: 9165296.
      Citations: 12     Fields:    Translation:AnimalsCells
    80. Shilton BH, Shuman HA, Mowbray SL. Crystal structures and solution conformations of a dominant-negative mutant of Escherichia coli maltose-binding protein. J Mol Biol. 1996 Nov 29; 264(2):364-76. PMID: 8951382.
      Citations: 13     Fields:    Translation:Cells
    81. Shuman HA, Horwitz MA. Legionella pneumophila invasion of mononuclear phagocytes. Curr Top Microbiol Immunol. 1996; 209:99-112. PMID: 8742248.
      Citations: 5     Fields:    Translation:HumansAnimalsCells
    82. Merino G, Boos W, Shuman HA, Bohl E. The inhibition of maltose transport by the unliganded form of the maltose-binding protein of Escherichia coli: experimental findings and mathematical treatment. J Theor Biol. 1995 Nov 21; 177(2):171-9. PMID: 8558904.
      Citations: 20     Fields:    Translation:Cells
    83. Bohl E, Shuman HA, Boos W. Mathematical treatment of the kinetics of binding protein dependent transport systems reveals that both the substrate loaded and unloaded binding proteins interact with the membrane components. J Theor Biol. 1995 Jan 07; 172(1):83-94. PMID: 7891451.
      Citations: 13     Fields:    Translation:Cells
    84. Brand BC, Sadosky AB, Shuman HA. The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages. Mol Microbiol. 1994 Nov; 14(4):797-808. PMID: 7891565.
      Citations: 89     Fields:    Translation:HumansCells
    85. Wiater LA, Marra A, Shuman HA. Escherichia coli F plasmid transfers to and replicates within Legionella pneumophila: an alternative to using an RP4-based system for gene delivery. Plasmid. 1994 Nov; 32(3):280-94. PMID: 7899513.
      Citations: 6     Fields:    Translation:Cells
    86. Sadosky AB, Wilson JW, Steinman HM, Shuman HA. The iron superoxide dismutase of Legionella pneumophila is essential for viability. J Bacteriol. 1994 Jun; 176(12):3790-9. PMID: 8206858; PMCID: PMC205569.
      Citations: 26     Fields:    Translation:Cells
    87. Covitz KM, Panagiotidis CH, Hor LI, Reyes M, Treptow NA, Shuman HA. Mutations that alter the transmembrane signalling pathway in an ATP binding cassette (ABC) transporter. EMBO J. 1994 Apr 01; 13(7):1752-9. PMID: 8157012; PMCID: PMC395008.
      Citations: 27     Fields:    Translation:Cells
    88. Wiater LA, Sadosky AB, Shuman HA. Mutagenesis of Legionella pneumophila using Tn903 dlllacZ: identification of a growth-phase-regulated pigmentation gene. Mol Microbiol. 1994 Feb; 11(4):641-53. PMID: 8196541.
      Citations: 53     Fields:    Translation:HumansCells
    89. Sadosky AB, Wiater LA, Shuman HA. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun. 1993 Dec; 61(12):5361-73. PMID: 8225610; PMCID: PMC281323.
      Citations: 177     Fields:    Translation:HumansCells
    90. Shuman HA, Panagiotidis CH. Tinkering with transporters: periplasmic binding protein-dependent maltose transport in E. coli. J Bioenerg Biomembr. 1993 Dec; 25(6):613-20. PMID: 7511584.
      Citations: 7     Fields:    Translation:HumansCells
    91. Panagiotidis CH, Reyes M, Sievertsen A, Boos W, Shuman HA. Characterization of the structural requirements for assembly and nucleotide binding of an ATP-binding cassette transporter. The maltose transport system of Escherichia coli. J Biol Chem. 1993 Nov 05; 268(31):23685-96. PMID: 8226895.
      Citations: 26     Fields:    Translation:Cells
    92. Hor LI, Shuman HA. Genetic analysis of periplasmic binding protein dependent transport in Escherichia coli. Each lobe of maltose-binding protein interacts with a different subunit of the MalFGK2 membrane transport complex. J Mol Biol. 1993 Oct 20; 233(4):659-70. PMID: 8411172.
      Citations: 26     Fields:    Translation:Cells
    93. Marra A, Blander SJ, Horwitz MA, Shuman HA. Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci U S A. 1992 Oct 15; 89(20):9607-11. PMID: 1409673; PMCID: PMC50181.
      Citations: 139     Fields:    Translation:AnimalsCells
    94. Dean DA, Hor LI, Shuman HA, Nikaido H. Interaction between maltose-binding protein and the membrane-associated maltose transporter complex in Escherichia coli. Mol Microbiol. 1992 Aug; 6(15):2033-40. PMID: 1406246.
      Citations: 17     Fields:    Translation:Cells
    95. Davidson AL, Shuman HA, Nikaido H. Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci U S A. 1992 Mar 15; 89(6):2360-4. PMID: 1549599; PMCID: PMC48657.
      Citations: 102     Fields:    Translation:Cells
    96. Marra A, Shuman HA. Genetics of Legionella pneumophila virulence. Annu Rev Genet. 1992; 26:51-69. PMID: 1482124.
      Citations: 11     Fields:    Translation:HumansCells
    97. Tapio S, Yeh F, Shuman HA, Boos W. The malZ gene of Escherichia coli, a member of the maltose regulon, encodes a maltodextrin glucosidase. J Biol Chem. 1991 Oct 15; 266(29):19450-8. PMID: 1918057.
      Citations: 26     Fields:    Translation:Cells
    98. Reyes M, Sievertsen A, Shuman HA, Boos W, Kühnau S. The activities of the Escherichia coli MalK protein in maltose transport, regulation, and inducer exclusion can be separated by mutations. J Bacteriol. 1991 Apr; 173(7):2180-6. PMID: 2007546; PMCID: PMC207765.
      Citations: 51     Fields:    Translation:Cells
    99. Campanelli D, Melchior M, Fu Y, Nakata M, Shuman H, Nathan C, Gabay JE. Cloning of cDNA for proteinase 3: a serine protease, antibiotic, and autoantigen from human neutrophils. J Exp Med. 1990 Dec 01; 172(6):1709-15. PMID: 2258701; PMCID: PMC2188764.
      Citations: 33     Fields:    Translation:HumansAnimalsCells
    100. Blander SJ, Szeto L, Shuman HA, Horwitz MA. An immunoprotective molecule, the major secretory protein of Legionella pneumophila, is not a virulence factor in a guinea pig model of Legionnaires' disease. J Clin Invest. 1990 Sep; 86(3):817-24. PMID: 2203824; PMCID: PMC296797.
      Citations: 23     Fields:    Translation:AnimalsCells
    101. Szeto L, Shuman HA. The Legionella pneumophila major secretory protein, a protease, is not required for intracellular growth or cell killing. Infect Immun. 1990 Aug; 58(8):2585-92. PMID: 2164510; PMCID: PMC258859.
      Citations: 35     Fields:    Translation:HumansCells
    102. Marra A, Horwitz MA, Shuman HA. The HL-60 model for the interaction of human macrophages with the Legionnaires' disease bacterium. J Immunol. 1990 Apr 01; 144(7):2738-44. PMID: 2138651.
      Citations: 35     Fields:    Translation:HumansCells
    103. Cianciotto N, Eisenstein BI, Engleberg NC, Shuman H. Genetics and molecular pathogenesis of Legionella pneumophila, an intracellular parasite of macrophages. Mol Biol Med. 1989 Oct; 6(5):409-24. PMID: 2696860.
      Citations: 27     Fields:    Translation:AnimalsCells
    104. McMorrow I, Shuman HA, Sze D, Wilson DM, Wilson TH. Sodium/proton antiport is required for growth of Escherichia coli at alkaline pH. Biochim Biophys Acta. 1989 May 19; 981(1):21-6. PMID: 2541789.
      Citations: 3     Fields:    Translation:Cells
    105. Marra A, Shuman HA. Isolation of a Legionella pneumophila restriction mutant with increased ability to act as a recipient in heterospecific matings. J Bacteriol. 1989 Apr; 171(4):2238-40. PMID: 2703472; PMCID: PMC209886.
      Citations: 20     Fields:    Translation:Cells
    106. Mintz CS, Shuman HA. Genetics of Legionella pneumophila. Microbiol Sci. 1988 Oct; 5(10):292-5. PMID: 2856299.
      Citations:    Fields:    Translation:HumansCells
    107. Reyes M, Shuman HA. Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J Bacteriol. 1988 Oct; 170(10):4598-602. PMID: 3049541; PMCID: PMC211497.
      Citations: 30     Fields:    Translation:Cells
    108. Treptow NA, Shuman HA. Allele-specific malE mutations that restore interactions between maltose-binding protein and the inner-membrane components of the maltose transport system. J Mol Biol. 1988 Aug 20; 202(4):809-22. PMID: 3050132.
      Citations: 32     Fields:    Translation:Cells
    109. Mintz CS, Chen JX, Shuman HA. Isolation and characterization of auxotrophic mutants of Legionella pneumophila that fail to multiply in human monocytes. Infect Immun. 1988 Jun; 56(6):1449-55. PMID: 3372016; PMCID: PMC259420.
      Citations: 37     Fields:    Translation:HumansCells
    110. Mintz CS, Shuman HA. Transposition of bacteriophage Mu in the Legionnaires disease bacterium. Proc Natl Acad Sci U S A. 1987 Jul; 84(13):4645-9. PMID: 3037523; PMCID: PMC305147.
      Citations: 4     Fields:    Translation:Cells
    111. Shuman HA. The genetics of active transport in bacteria. Annu Rev Genet. 1987; 21:155-77. PMID: 3327461.
      Citations: 12     Fields:    Translation:Cells
    112. Reyes M, Treptow NA, Shuman HA. Transport of p-nitrophenyl-alpha-maltoside by the maltose transport system of Escherichia coli and its subsequent hydrolysis by a cytoplasmic alpha-maltosidase. J Bacteriol. 1986 Mar; 165(3):918-22. PMID: 3512530; PMCID: PMC214516.
      Citations: 15     Fields:    Translation:Cells
    113. Treptow NA, Shuman HA. Genetic evidence for substrate and periplasmic-binding-protein recognition by the MalF and MalG proteins, cytoplasmic membrane components of the Escherichia coli maltose transport system. J Bacteriol. 1985 Aug; 163(2):654-60. PMID: 3894331; PMCID: PMC219172.
      Citations: 50     Fields:    Translation:Cells
    114. Shuman HA. Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J Biol Chem. 1982 May 25; 257(10):5455-61. PMID: 7040366.
      Citations: 68     Fields:    Translation:Cells
    115. Shuman HA. The maltose-maltodextrin transport system of Escherichia coli. Ann Microbiol (Paris). 1982 Jan; 133A(1):153-9. PMID: 7041738.
      Citations: 11     Fields:    Translation:Cells
    116. Boos W, Ferenci T, Shuman HA. Formation and excretion of acetylmaltose after accumulation of maltose in Escherichia coli. J Bacteriol. 1981 May; 146(2):725-32. PMID: 7012137; PMCID: PMC217018.
      Citations: 7     Fields:    Translation:Cells
    117. Shuman HA, Silhavy TJ. Identification of the malK gene product. A peripheral membrane component of the Escherichia coli maltose transport system. J Biol Chem. 1981 Jan 25; 256(2):560-2. PMID: 6778869.
      Citations: 40     Fields:    Translation:Cells
    118. Shuman HA. The use of gene fusions of study bacterial transport proteins. J Membr Biol. 1981; 61(1):1-11. PMID: 6267284.
      Citations: 4     Fields:    
    119. Shuman HA, Silhavy TJ, Beckwith JR. Labeling of proteins with beta-galactosidase by gene fusion. Identification of a cytoplasmic membrane component of the Escherichia coli maltose transport system. J Biol Chem. 1980 Jan 10; 255(1):168-74. PMID: 6765939.
      Citations: 51     Fields:    Translation:Cells
    120. Silhavy TJ, Brickman E, Bassford PJ, Casadaban MJ, Shuman HA, Schwartz V, Guarente L, Schwartz M, Beckwith JR. Structure of the malB region in Escherichia coli K12. II. Genetic map of the malE,F,G operon. Mol Gen Genet. 1979 Jul 24; 174(3):249-59. PMID: 384167.
      Citations: 55     Fields:    Translation:Cells
    121. Brickman E, Silhavy TJ, Bassford PJ, Shuman HA, Beckwith JR. Sites within gene lacZ of Escherichia coli for formation of active hybrid beta-galactosidase molecules. J Bacteriol. 1979 Jul; 139(1):13-8. PMID: 110776; PMCID: PMC216821.
      Citations: 15     Fields:    Translation:Cells
    122. Shuman HA, Beckwith J. Escherichia coli K-12 mutants that allow transport of maltose via the beta-galactoside transport system. J Bacteriol. 1979 Jan; 137(1):365-73. PMID: 368019; PMCID: PMC218459.
      Citations: 17     Fields:    Translation:Cells
    123. Shuman HA, Silhavy TJ, Schwartz M, Débarbouillé M. Dominant constitutive mutations in malT, the positive regulator gene of the maltose regulon in Escherichia coli. J Mol Biol. 1978 Sep 15; 124(2):359-71. PMID: 101676.
      Citations: 73     Fields:    Translation:Cells
    124. Silhavy TJ, Shuman HA, Beckwith J, Schwartz M. Use of gene fusions to study outer membrane protein localization in Escherichia coli. Proc Natl Acad Sci U S A. 1977 Dec; 74(12):5411-5. PMID: 414221; PMCID: PMC431741.
      Citations: 70     Fields:    Translation:Cells
    125. Somlyo AV, Shuman H, Somlyo AP. Composition of sarcoplasmic reticulum in situ by electron probe X-ray microanalysis. Nature. 1977 Aug 11; 268(5620):556-8. PMID: 887175.
      Citations: 41     Fields:    Translation:AnimalsCells
    126. Silhavy TJ, Casadaban MJ, Shuman HA, Beckwith JR. Conversion of beta-galactosidase to a membrane-bound state by gene fusion. Proc Natl Acad Sci U S A. 1976 Oct; 73(10):3423-7. PMID: 790385; PMCID: PMC431127.
      Citations: 49     Fields:    Translation:Cells
    127. Shuman H, Somlyo AP. Electron probe x-ray analysis of single ferritin molecules. Proc Natl Acad Sci U S A. 1976 Apr; 73(4):1193-5. PMID: 1063401; PMCID: PMC430227.
      Citations: 4     Fields:    
    128. Shuman H, Schwartz M. The effect of nalidixic acid on the expression of some genes in Escherichia coli K-12. Biochem Biophys Res Commun. 1975 May 05; 64(1):204-9. PMID: 167732.
      Citations: 24     Fields:    Translation:Cells
    129. Ryter A, Shuman H, Schwartz M. Intergration of the receptor for bacteriophage lambda in the outer membrane of Escherichia coli: coupling with cell division. J Bacteriol. 1975 Apr; 122(1):295-301. PMID: 164434; PMCID: PMC235669.
      Citations: 44     Fields:    Translation:Cells
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