Germinal centre hypoxia and regulation of antibody qualities by a hypoxia response system

Nature

Volumn 537, Issue 7619, 2016, Pages 234-238

  Cho, Sung Hoon ^a   Raybuck, Ariel L ^a   Stengel, Kristy ^b   Wei, Mei ^a   Beck, Thomas C ^a   Volanakis, Emmanuel ^a   Thomas, James W ^a   Hiebert, Scott ^b,c   Haase, Volker H ^a,b,c,d   Boothby, Mark R ^a,b,c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2C; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; UNCLASSIFIED DRUG; CYTOSINE DEAMINASE; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ANTIBODY; ANTIGEN; CELLS AND CELL COMPONENTS; CLONE; GENE EXPRESSION; GROWTH RESPONSE; HYPOXIA; IMMUNITY; PHYSIOLOGY; PROTEIN; TUMOR; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL EXPANSION; CELL FUNCTION; CELL HYPOXIA; CELL LOSS; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION; GERMINAL CENTER; HUMORAL IMMUNITY; IMMUNE RESPONSE; MEMORY CELL; MOUSE; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; C57BL MOUSE; CELL SURVIVAL; CYTOLOGY; GENE REARRANGEMENT; HYPOXIA; IMMUNOLOGY; METABOLISM;

MUS;

ANIMALS; ANTIBODIES; B-LYMPHOCYTES; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; CYTOSINE DEAMINASE; GERMINAL CENTER; HYPOXIA; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; TOR SERINE-THREONINE KINASES;

EID: 84986575883     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19334     Document Type: Article

References (35)

1. Victora, G. D., Nussenzweig, M. C. Germinal centers. Annu. Rev. Immunol. 30, 429-457 (2012).
2. Shlomchik, M. J., Weisel, F. Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 247, 52-63 (2012).
3. Xu, Z., Zan, H., Pone, E. J., Mai, T., Casali, P. Immunoglobulin class-switch DNA recombination: induction, targeting and beyond. Nat. Rev. Immunol. 12, 517-531 (2012).
4. Stavnezer, J., Guikema, J. E., Schrader, C. E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292 (2008).
5. Cui, G. et al. IL-7-induced glycerol transport and TAG synthesis promotes memory CD8+ T cell longevity. Cell 161, 750-761 (2015).
6. Munn, D. H. et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193 (1998).
7. Kaelin, W. G. Jr. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer 8, 865-873 (2008).
8. Pearce, E. L., Poffenberger, M. C., Chang, C. H., Jones, R. G. Fueling immunity: insights into metabolism and lymphocyte function. Science 342, 1242454 (2013).
9. Spencer, J. A. et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 508, 269-273 (2014).
10. Patten, D. A. et al. Hypoxia-inducible factor-1 activation in nonhypoxic conditions: the essential role of mitochondrial-derived reactive oxygen species. Mol. Biol. Cell 21, 3247-3257 (2010).
11. Koch, C. J. Importance of antibody concentration in the assessment of cellular hypoxia by flow cytometry: EF5 and pimonidazole. Radiat. Res. 169, 677-688 (2008).
12. Colgan, S. P., Taylor, C. T. Hypoxia: an alarm signal during intestinal inflammation. Nat. Rev. Gastroenterol. Hepatol. 7, 281-287 (2010).
13. Rush, J. S., Liu, M., Odegard, V. H., Unniraman, S., Schatz, D. G. Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination. Proc. Natl Acad. Sci. USA 102, 13242-13247 (2005).
14. Peng, S. L., Szabo, S. J., Glimcher, L. H. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl Acad. Sci. USA 99, 5545-5550 (2002).
15. Kaelin, W. G. Jr & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402 (2008).
16. Bannard, O. et al. Germinal center centroblasts transition to a centrocyte phenotype according to a timed program and depend on the dark zone for effective selection. Immunity 39, 912-924 (2013).
17. Wouters, B. G., Koritzinsky, M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer 8, 851-864 (2008).
18. Krymskaya, V. P. et al. mTOR is required for pulmonary arterial vascular smooth muscle cell proliferation under chronic hypoxia. FASEB J. 25, 1922-1933 (2011).
19. Keating, R. et al. The kinase mTOR modulates the antibody response to provide cross-protective immunity to lethal infection with influenza virus. Nat. Immunol. 14, 1266-1276 (2013).
20. Zhang, S. et al. B cell-specific deficiencies in mTOR limit humoral immune responses. J. Immunol. 191, 1692-1703 (2013).
21. Laplante, M., Sabatini, D. M. mTOR signaling in growth control and disease. Cell 149, 274-293 (2012).
22. Nimmerjahn, F., Ravetch, J. V. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310, 1510-1512 (2005).
23. O'Keeffe, S. et al. Immunoglobulin G subclasses and spirometry in patients with chronic obstructive pulmonary disease. Eur. Respir. J. 4, 932-936 (1991).
24. Gabrilovich, D. I. et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 2, 1096-1103 (1996).
25. Hatfield, S. M. et al. Immunological mechanisms of the antitumor effects of supplemental oxygenation. Sci. Transl. Med. 7, 277-30 (2015).
26. Konisti, S., Kiriakidis, S., Paleolog, E. M. Hypoxia-a key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat. Rev. Rheumatol. 8, 153-162 (2012).
27. Eltzschig, H. K., Carmeliet, P. Hypoxia and inflammation. N. Engl. J. Med. 364, 656-665 (2011).
28. Karhausen, J. et al. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114, 1098-1106 (2004).
29. Liu, Q., Davidoff, O., Niss, K., Haase, V. H. Hypoxia-inducible factor regulates hepcidin via erythropoietin-induced erythropoiesis. J. Clin. Invest. 122, 4635-4644 (2012).
30. Guertin, D. A. et al. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKC?, but not S6K1. Dev. Cell 11, 859-871 (2006).
31. Woods, M. L., Koch, C. J., Lord, E. M. Detection of individual hypoxic cells in multicellular spheroids by flow cytometry using the 2-nitroimidazole, EF5, and monoclonal antibodies. Int. J. Radiat. Oncol. Biol. Phys. 34, 93-101 (1996).
32. Cho, S. H. et al. Glycolytic rate and lymphomagenesis depend on PARP14, an ADP ribosyltransferase of the B aggressive lymphoma (BAL) family. Proc. Natl Acad. Sci. USA 108, 15972-15977 (2011).
33. Cho, S. H. et al. B cell-intrinsic and-extrinsic regulation of antibody responses by PARP14, an intracellular (ADP-ribosyl)transferase. J. Immunol. 191, 3169-3178 (2013).
34. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protocols 7, 562-578 (2012).
35. Eustace, A. et al. A 26-gene hypoxia signature predicts benefit from hypoxiamodifying therapy in laryngeal cancer but not bladder cancer. Clin. Cancer Res. 19, 4879-4888 (2013).