Functionally significant metabolic differences between B and T lymphocyte lineages

被引:22
作者
Khalsa, Jasneet Kaur [1 ,5 ]
Chawla, Amanpreet Singh [1 ,6 ]
Prabhu, Savit B. [2 ]
Vats, Mukti [1 ,7 ]
Dhar, Atika [1 ]
Dev, Gagan [1 ]
Das, Nabanita [3 ,8 ]
Mukherjee, Sandip [3 ,9 ]
Tanwar, Shalini [1 ,10 ]
Banerjee, Hridesh [1 ,11 ]
Durdik, Jeannine Marie [4 ]
Bal, Vineeta [1 ]
George, Anna [1 ]
Rath, Satyajit [1 ]
Arimbasseri, Gopalakrishnan Aneeshkumar [1 ]
机构
[1] Natl Inst Immunol, Aruna Asaf Ali Rd, New Delhi 110067, India
[2] Christian Med Coll & Hosp, Wellcome Lab, Vellore, Tamil Nadu, India
[3] Indian Inst Chem Biol, Kolkata, India
[4] Univ Arkansas, Dept Biol Sci, Fayetteville, AR 72701 USA
[5] Harvard Med Sch, Ctr Stem Cell Therapeut & Imaging, Boston, MA 02115 USA
[6] Cincinnati Childrens Hosp Med Ctr, Div Immunobiol, Cincinnati, OH 45229 USA
[7] Indian Inst Technol, Dept Biosci & Bioengn, Mumbai, Maharashtra, India
[8] Cent Drug Res Inst, Biochem Div, Lucknow, Uttar Pradesh, India
[9] Baylor Inst Immunol Res, Dallas, TX USA
[10] NIAID, Cellular Immunol Sect, Lab Immune Syst Biol, 9000 Rockville Pike, Bethesda, MD 20892 USA
[11] Univ Pittsburgh, Sch Med, Dept Immunol, Pittsburgh, PA USA
关键词
B-cells; metabolic differences; ribo-seq; RNA-seq; T-cells; APOPTOSIS-INDUCING-FACTOR; SET ENRICHMENT ANALYSIS; MITOCHONDRIAL-FUNCTION; CELL-DEVELOPMENT; PRO-B; TRANSLATION; ACTIVATION; MOTILITY; DIFFERENTIATION; IDENTIFICATION;
D O I
10.1111/imm.13098
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
071005 [微生物学]; 100108 [医学免疫学];
摘要
Activation of B and T lymphocytes leads to major remodelling of the metabolic landscape of the cells enabling their post-activation functions. However, naive B and T lymphocytes also show metabolic differences, and the genesis, nature and functional significance of these differences are not yet well understood. Here we show that resting B-cells appeared to have lower energy demands than resting T-cells as they consumed lower levels of glucose and fatty acids and produced less ATP. Resting B-cells are more dependent on OXPHOS, while T-cells show more dependence on aerobic glycolysis. However, despite an apparently higher energy demand, T lineage cells showed lower rates of protein synthesis than equivalent B lineage stages. These metabolic differences between the two lineages were established early during lineage differentiation, and were functionally significant. Higher levels of protein synthesis in B-cells were associated with increased synthesis of MHC class II molecules and other proteins associated with antigen internalization, transport and presentation. The combination of higher energy demand and lower protein synthesis in T-cells was consistent with their higher ATP-dependent motility. Our data provide an integrated perspective of the metabolic differences and their functional implications between the B and T lymphocyte lineages.
引用
收藏
页码:104 / 120
页数:17
相关论文
共 75 条
[1]
HTSeq-a Python']Python framework to work with high-throughput sequencing data [J].
Anders, Simon ;
Pyl, Paul Theodor ;
Huber, Wolfgang .
BIOINFORMATICS, 2015, 31 (02) :166-169
[2]
Translation is actively regulated during the differentiation of CD8+ effector T cells [J].
Araki, Koichi ;
Morita, Masahiro ;
Bederman, Annelise G. ;
Konieczny, Bogumila T. ;
Kissick, Haydn T. ;
Sonenberg, Nahum ;
Ahmed, Rafi .
NATURE IMMUNOLOGY, 2017, 18 (09) :1046-+
[3]
Gene Ontology: tool for the unification of biology [J].
Ashburner, M ;
Ball, CA ;
Blake, JA ;
Botstein, D ;
Butler, H ;
Cherry, JM ;
Davis, AP ;
Dolinski, K ;
Dwight, SS ;
Eppig, JT ;
Harris, MA ;
Hill, DP ;
Issel-Tarver, L ;
Kasarskis, A ;
Lewis, S ;
Matese, JC ;
Richardson, JE ;
Ringwald, M ;
Rubin, GM ;
Sherlock, G .
NATURE GENETICS, 2000, 25 (01) :25-29
[4]
Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes [J].
Bajenoff, Marc ;
Egen, Jackson G. ;
Koo, Lily Y. ;
Laugier, Jean Pierre ;
Brau, Frederic ;
Glaichenhaus, Nicolas ;
Germain, Ronald N. .
IMMUNITY, 2006, 25 (06) :989-1001
[5]
Modulation of Naive CD8 T Cell Response Features by Ligand Density, Affinity, and Continued Signaling via Internalized TCRs [J].
Balyan, Renu ;
Gund, Rupali ;
Ebenezer, Chitra ;
Khalsa, Jasneet Kaur ;
Verghese, Divya Anna ;
Krishnamurthy, Thyagarajan ;
George, Anna ;
Bal, Vineeta ;
Rath, Satyajit ;
Chaudhry, Ashutosh .
JOURNAL OF IMMUNOLOGY, 2017, 198 (05) :1823-1837
[6]
A role for apoptosis-inducing factor in T cell development [J].
Banerjee, Hridesh ;
Das, Abhishek ;
Srivastava, Smita ;
Mattoo, Hamid R. ;
Thyagarajan, Krishnamurthy ;
Khalsa, Jasneet Kaur ;
Tanwar, Shalini ;
Das, Deepika Sharma ;
Majumdar, Subeer S. ;
George, Anna ;
Bal, Vineeta ;
Durdik, Jeannine M. ;
Rath, Satyajit .
JOURNAL OF EXPERIMENTAL MEDICINE, 2012, 209 (09) :1641-1653
[7]
Distinct Translational Control in CD4+ T Cell Subsets [J].
Bjur, Eva ;
Larsson, Ola ;
Yurchenko, Ekaterina ;
Zheng, Lei ;
Gandin, Valentina ;
Topisirovic, Ivan ;
Li, Shui ;
Wagner, Carston R. ;
Sonenberg, Nahum ;
Piccirillo, Ciriaco A. .
PLOS GENETICS, 2013, 9 (05)
[8]
Estimating the precursor frequency of naive antigen-specific CD8 T cells [J].
Blattman, JN ;
Antia, R ;
Sourdive, DJD ;
Wang, XC ;
Kaech, SM ;
Murali-Krishna, K ;
Altman, JD ;
Ahmed, R .
JOURNAL OF EXPERIMENTAL MEDICINE, 2002, 195 (05) :657-664
[9]
Metabolic Regulation of the Immune Humoral Response [J].
Boothby, Mark ;
Rickert, Robert C. .
IMMUNITY, 2017, 46 (05) :743-755
[10]
A HIERARCHY OF ATP-CONSUMING PROCESSES IN MAMMALIAN-CELLS [J].
BUTTGEREIT, F ;
BRAND, MD .
BIOCHEMICAL JOURNAL, 1995, 312 :163-167