Ann Haberman, PhD
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Research Summary
I am interested in understanding the factors that influence the proliferation, migration and differentiation of germinal center B lymphocytes. A particular interest of mine is the behavior of activated B cells and their interaction with other cell types within the context of tissue architecture. I use a combination of histology, flow cytometry and intravital multiphoton microscopy to study the factors that regulate B cell subset activation and their movements in vivo. A related area of interest includes the cellular interactions of B cell lymphomas with other cell types within lymphoma microenvironments that may influence lymphoma resistance to therapeutic treatments.
Extensive Research Description
My research has focused on the cellular and molecular interactions regulating the form and function of an inducible lymphoid tissue structure called germinal centers. Germinal centers (GC) develop in the center of B cell follicles in spleen and lymph nodes about one week after initial immunization. GCs are sites of extreme metabolism, with very high proliferation and death rates, and evolve over time to form structures with phenotypically distinct zones. GC development requires intricate interactions of B cells with multiple other cell types to achieve both the affinity maturation of immunoglobulin and the generation of memory B cells that are key to long-term immune protection.
Several lymphoma subtypes derive from germinal centers, including diffuse large B cell lymphomas, follicular lymphomas and angioImmunoblastic T cell lymphomas. The regional composition of other cell types can vary tremendously and can include CD4+ T cell subsets, dendritic cells and activated macrophages. Defining the impact of interactions with other adjacent cell types will be an essential component of advances in this field. My current research aims to tease apart the role that each may play in the cascade of events regulating the pathological variants of germinal centers.
Coauthors
Research Interests
Antibody Formation; Immunity, Cellular; Lymphocyte Activation; Lymphoid Tissue; Lymphoma, Follicular; Lymphoma, B-Cell; Germinal Center; Dendritic Cells, Follicular; Immunological Synapses
Public Health Interests
Immunology
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Selected Publications
- Germinal center B cell development has distinctly regulated stages completed by disengagement from T cell help.Zhang TT, Gonzalez DG, Cote CM, Kerfoot SM, Deng S, Cheng Y, Magari M, Haberman AM. Germinal center B cell development has distinctly regulated stages completed by disengagement from T cell help. ELife 2017, 6 PMID: 28498098, PMCID: PMC5429091, DOI: 10.7554/eLife.19552.
- Preclinical Advances with Multiphoton Microscopy in Live Imaging of Skin Cancers.Sun TY, Haberman AM, Greco V. Preclinical Advances with Multiphoton Microscopy in Live Imaging of Skin Cancers. The Journal Of Investigative Dermatology 2017, 137: 282-287. PMID: 27847119, PMCID: PMC5258832, DOI: 10.1016/j.jid.2016.08.033.
- Tissue-scale coordination of cellular behaviour promotes epidermal wound repair in live mice.Park S, Gonzalez DG, Guirao B, Boucher JD, Cockburn K, Marsh ED, Mesa KR, Brown S, Rompolas P, Haberman AM, Bellaïche Y, Greco V. Tissue-scale coordination of cellular behaviour promotes epidermal wound repair in live mice. Nature Cell Biology 2017, 19: 155-163. PMID: 28248302, PMCID: PMC5581297, DOI: 10.1038/ncb3472.
- Intravital imaging of hair follicle regeneration in the mouse.Pineda CM, Park S, Mesa KR, Wolfel M, Gonzalez DG, Haberman AM, Rompolas P, Greco V. Intravital imaging of hair follicle regeneration in the mouse. Nature Protocols 2015, 10: 1116-30. PMID: 26110716, PMCID: PMC4632978, DOI: 10.1038/nprot.2015.070.
- Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool.Mesa KR, Rompolas P, Zito G, Myung P, Sun TY, Brown S, Gonzalez DG, Blagoev KB, Haberman AM, Greco V. Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool. Nature 2015, 522: 94-7. PMID: 25849774, PMCID: PMC4457634, DOI: 10.1038/nature14306.
- The BCL6 RD2 domain governs commitment of activated B cells to form germinal centers.Huang C, Gonzalez DG, Cote CM, Jiang Y, Hatzi K, Teater M, Dai K, Hla T, Haberman AM, Melnick A. The BCL6 RD2 domain governs commitment of activated B cells to form germinal centers. Cell Reports 2014, 8: 1497-508. PMID: 25176650, PMCID: PMC4163070, DOI: 10.1016/j.celrep.2014.07.059.
- Dynamic expression of BCL6 in murine conventional dendritic cells during in vivo development and activation.Zhang TT, Liu D, Calabro S, Eisenbarth SC, Cattoretti G, Haberman AM. Dynamic expression of BCL6 in murine conventional dendritic cells during in vivo development and activation. PloS One 2014, 9: e101208. PMID: 24979752, PMCID: PMC4076320, DOI: 10.1371/journal.pone.0101208.
- What ticks do under your skin: two-photon intravital imaging of Ixodes scapularis feeding in the presence of the lyme disease spirochete.Bockenstedt LK, Gonzalez D, Mao J, Li M, Belperron AA, Haberman A. What ticks do under your skin: two-photon intravital imaging of Ixodes scapularis feeding in the presence of the lyme disease spirochete. The Yale Journal Of Biology And Medicine 2014, 87: 3-13. PMID: 24600332, PMCID: PMC3941458.
- Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner.King IL, Fortier A, Tighe M, Dibble J, Watts GF, Veerapen N, Haberman AM, Besra GS, Mohrs M, Brenner MB, Leadbetter EA. Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nature Immunology 2011, 13: 44-50. PMID: 22120118, PMCID: PMC3833037, DOI: 10.1038/ni.2172.
- Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration.Rompolas P, Deschene ER, Zito G, Gonzalez DG, Saotome I, Haberman AM, Greco V. Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature 2012, 487: 496-9. PMID: 22763436, PMCID: PMC3772651, DOI: 10.1038/nature11218.
- Spirochete antigens persist near cartilage after murine Lyme borreliosis therapy.Bockenstedt LK, Gonzalez DG, Haberman AM, Belperron AA. Spirochete antigens persist near cartilage after murine Lyme borreliosis therapy. The Journal Of Clinical Investigation 2012, 122: 2652-60. PMID: 22728937, PMCID: PMC3386809, DOI: 10.1172/JCI58813.
- In vivo imaging of virological synapses.Sewald X, Gonzalez DG, Haberman AM, Mothes W. In vivo imaging of virological synapses. Nature Communications 2012, 3: 1320. PMID: 23271654, PMCID: PMC3784984, DOI: 10.1038/ncomms2338.
- Combination delivery of TGF-β inhibitor and IL-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy.Park J, Wrzesinski SH, Stern E, Look M, Criscione J, Ragheb R, Jay SM, Demento SL, Agawu A, Licona Limon P, Ferrandino AF, Gonzalez D, Habermann A, Flavell RA, Fahmy TM. Combination delivery of TGF-β inhibitor and IL-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy. Nature Materials 2012, 11: 895-905. PMID: 22797827, PMCID: PMC3601683, DOI: 10.1038/nmat3355.
- Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone.Kerfoot SM, Yaari G, Patel JR, Johnson KL, Gonzalez DG, Kleinstein SH, Haberman AM. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011, 34: 947-60. PMID: 21636295, PMCID: PMC3280079, DOI: 10.1016/j.immuni.2011.03.024.
- Cellular choreography in the germinal center: new visions from in vivo imaging.Hauser AE, Kerfoot SM, Haberman AM. Cellular choreography in the germinal center: new visions from in vivo imaging. Seminars In Immunopathology 2010, 32: 239-55. PMID: 20614218, PMCID: PMC3659422, DOI: 10.1007/s00281-010-0214-z.
- In vivo imaging studies shed light on germinal-centre development.Hauser AE, Shlomchik MJ, Haberman AM. In vivo imaging studies shed light on germinal-centre development. Nature Reviews. Immunology 2007, 7: 499-504. PMID: 17589541, DOI: 10.1038/nri2120.
- Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns.Hauser AE, Junt T, Mempel TR, Sneddon MW, Kleinstein SH, Henrickson SE, von Andrian UH, Shlomchik MJ, Haberman AM. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 2007, 26: 655-67. PMID: 17509908, DOI: 10.1016/j.immuni.2007.04.008.