eISSN: 1644-4124
ISSN: 1426-3912
Central European Journal of Immunology
Current issue Archive Manuscripts accepted About the journal Abstracting and indexing Subscription Contact Instructions for authors
SCImago Journal & Country Rank

vol. 43
Review paper

Immunological memory cells

Weronika Ratajczak, Paulina Niedźwiedzka-Rystwej, Beata Tokarz-Deptuła, Wiesław Deptuła

(Centr Eur Immunol 2018; 43 (2): 194-203)
Online publish date: 2018/06/30
View full text
Get citation
JabRef, Mendeley
Papers, Reference Manager, RefWorks, Zotero
This article reviews immunological memory cells, currently represented by T and B lymphocytes and natural killer (NK) cells, which determine a rapid and effective response against a second encounter with the same antigen. Among T lymphocytes, functions of memory cells are provided by their subsets: central memory, effector memory, tissue-resident memory, regulatory memory and stem memory T cells. Memory T and B lymphocytes have an essential role in the immunity against microbial pathogens but are also involved in autoimmunity and maternal-fetal tolerance. Furthermore, the evidence of immunological memory has been established for NK cells. NK cells can respond to haptens or viruses, which results in generation of antigen-specific memory cells.

T, B and NK cells, which have a role in immunological memory, have been characterized phenotypically and functionally. During the secondary immune response, these cells are involved in the reaction against foreign antigens, including pathogens, and take part in autoimmune diseases, but also are crucial to immunological tolerance and vaccine therapy.

immunological memory, memory T cells, memory B cells, memory NK cells

Niedźwiedzka-Rystwej P, Tokarz-Deptuła B, Deptuła W (2013): Charakterystyka subpopulacji limfocytów T. Postepy Hig Med Dosw 67: 371-379.
Gasper DJ, Tejera MM, Suresh M (2014): CD4 T-cell generation and maintenance. Crit Rev Immunol 34: 121-146.
Valbon SF, Condotta SA, Richer MJ (2016): Regulation of effector and memory CD8+ T cell function by inflammatory cytokines. Cytokine 82: 16-23.
Golubovskaya V, Wu L (2016): Different subsets of T cells, memory, effector functions and CAR-T immunotherapy. Cancers 8: 36.
Flynn JK, Gorry PR (2014): Stem memory T cells (TSCM) – their role in cancer and HIV immunotherapies. Clin Transl Immunology 3: 1-7.
Gattinoni L, Lugli E, Ji Y, et al. (2011): A human memory T cell subset with stem cell-like properties. Nat Med 17: 1290-1297.
Busch DH, Fräßle SP, Sommermeyer D, et al. (2016): Role of memory T cell subsets for adoptive immunotherapy. Semin Immunol 28: 28-34.
Sallusto F, Geginat J, Lanzavecchia A (2004): Central memory and effector memory T cell subsets: function, generation and maintenance. Annu Rev Immunol 22: 745-763.
Faint JM, Annels NE, Curnow SJ, et al. (2001): Memory T cells constitute a subset of the human CD8+CD45RA+ pool with distinct phenotypic and migratory characteristics. J Immunol 167: 212-220.
Rosado MM, Scarsella M, Pandolfi E, et al. (2011): Switched memory B cells maintain specific memory independent of serum antibodies: The hepatitis B example. Eur J Immunol 41: 1800-1808.
Sage AP, Mallat Z (2014): Multiple potential roles for B cells in atherosclerosis. Ann Med 46: 297-303.
Ahlers JD, Belyakov IM (2010): Memories that last forever: strategies for optimizing vaccine T-cell memory. Blood 115: 1678-1689.
Zhang Q, Lakkis FG (2015): Memory T cell migration. Front Immunol 6: 504.
Roberts AD, Ely KH, Woodland DL (2005): Differential contributions of central and effector memory T cells to recall responses. J Exp Med 202: 123-133.
Borges de Silva H, Fonseca R, Alvarez JM, et al. (2015): IFN priming effects on the maintenance of effector memory CD4+ T cells and phagocyte function: evidence from infectious disease. J Immunol Res 3: 1-8.
Tubo NJ, Fife BT, Pagan AJ, et al. (2016): Most microbe – specific naïve CD4+ T cells produce memory cells during infection. Science 351: 511-514.
Martin MD, Kim MT, Shan Q, et al. (2015): Phenotypic and functional alterations in circulating memory CD8 T cells with time after primary infection. PLoS Pathog 11: e1005219.
Zhao J, Zhao J, Managalam AK, et al. (2016): Airway memory CD4+ T cells mediate protective immunity against emerging respiratory coronaviruses. Immunity 44: 1379-1391.
Balmer ML, Ma EH, Bantug GR, et al. (2016): Memory CD8+ T cells require increased concentrations of acetate induced by stress for optimal function. Immunity 44: 1-13.
MacLeod MKL, Kappler JW, Marrack P (2010): Memory CD4 T cells: generation, reactivation and re-assignment. Immunology 130: 10-15.
Carbone FR (2015): Tissue-resident memory T cells and fixed immune surveillance in nonlymphoid organs. J Immunol 195: 17-22.
Clark RA (2015): Resident memory T cells in human health and disease. Sci Transl Med 7: 1-8.
Shin H, Iwasaki A (2013): Tissue-resident memory T cells. Immunol Rev 255: 165-181.
Mueller SN, Mackay LK (2016): Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol 16: 79-89.
Mackay LK, Rahimpour A, Ma JZ, et al. (2013): The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin. Nat Immunol 14: 1294-1301.
Casey KA, Fraser KA, Schenkel JM, et al. (2012): Antigen independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188: 4866-4875.
Thom JT, Oxenius A (2016): Tissue-resident memory T cells in cytomegalovirus. Curr Opin Virol 16: 63-69.
Ritzel RM, Crapser J, Patel AR, et al. (2016): Age-associated resident memory CD8 T cells in the central nervous system are primed to potentiate inflammation after ischemic brain injury. J Immunol 196: 3318-3330.
Mackay LK, Kallies A (2016): Transcriptional regulation of tissue-resident lymphocytes. Trends Immunol 38: 94-103.
Turner DL, Farber DL (2014): Mucosal resident memory CD4 T cells in protection and immunopathology. Front Immunol 5: 331.
Glennie ND, Yeramilli VA, Beiting DP, et al. (2015): Skin-resident memory CD4+ T cells enhance protection against Leishmania major infection. J Exp. Med 212: 1405-1414.
Teijaro JR, Turner D, Pham Q, et al. (2011): Cutting edge: tissue-retentive lung memor CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 187: 5510-5514.
Turner DL, Bickham KL, Thome JJ, et al. (2014): Lung niches for the generation and maintenance of tissue-resident memory T cells. Mucosal Immunol 7: 501-510.
Adachi T, Kobayashi T, Sugihara E, et al. (2015): Hair-follicle-derived IL-17 and IL-15 mediate skin-resident memory T cell homeostasis and lymphoma. Nat Med 21: 1272-1279.
Di Rosa F, Gebhardt T (2016): Bone marrow T cells and the integrated functions of recirculaying and tissue-resient memory T cells. Front Immunol 7: 1-13.
Park CO, Kupper TS (2015): The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat Med 21: 688-697.
Adamiak M, Tokarz-Deptuła B, Deptuła W (2014): Charakterystyka naturalnych komórek limfoidalnych (ILC). Postepy Hig Med Dosw 68: 1464-1471.
Martinez-Gonzalez I, Matha L, Steer A., Tahei F (2017): Immunological memory of group 2 innate lymphoid cells. Trends Immunol 38: 423-431.
Laidlaw BJ, Craft JE, Kaech SM (2016): The multifaced role of CD4+ T cells in CD8+ T cell memory. Nat Rev Immunol 16: 102-111.
Soerens AG, Costa AD, Lind JM (2016): Regulatory T cells are essential to promote proper CD4 T-cell priming upon mucosal infection. Mucosal Immunol 9: 1395-1406.
Vignali DAA, Collison LW, Workman CJ (2008): How regulatory T cells work. Nat Rev Immunol 8: 523-532.
Chen X, Du Y, Lin X, et al. (2016): CD4+CD25+ regulatory T cells in tumor immunity. Int Immunopharmacol 34: 244-249.
Ito T, Yamada A, Batal I, et al. (2016): The limits of linked suppression for regulatory T cells. Front Immunol 7: 1-4.
Su J, Xie Q, Xu Y, et al. (2015): Role of CD8+ regulatory T cells in organ transplantation. Burns&Trauma 2: 18-23.
Schmitt EG, Williams CB (2013): Generation and function of induced regulatory T cells. Front Immunol 4: 152.
Hilbrands R, Chen Y, Kendal AR, et al. (2016): Induced Foxp3+ T cells colonizing tolerated allografts exhibit the hypomethylation pattern typical of mature regulation T cells. Front Immunol 7: 1-8.
Tanoue T, Atarashi K, Honda K (2016): Development and maintenance of intestinal regulatory T cells. Nat Rev Immunol 16: 295-309.
Ng WF, Duggan PJ, Ponchel F, et al. (2001): Human CD4+CD25+ cells: a naturally occurrting populations of regulatory T cells. Blood 98: 2736-2744.
Vinay DS, Kim CH, Choi BK, Kwon BS (2009): Origins and functional basis of regulatory CD11c+CD8+ T cells. Eur J Immunol 39: 1552-1563.
Sanchez AM, Yang Y (2011): The role of natural regulatory T cells in infection. Immunol Res 49: 124-134.
Feuerer M, Hill JA, Mathis D, Benoist C (2009): Foxp3+ regulatory T cells: differentiation, specificification, subphenotypes. Nat Immunol 10: 689-696.
Wing K, Sakaguchi S (2010): Regulatory T cells exert checks and balances on self-tolerance and autoimmunity. Nat Immunol 11: 7-13.
Sun L, Jin H, Li H (2016): GARP: a surface molecule of regulatory T cells that is involved in the regulatory function and TGF releasing. Oncotarget 7: 42826-42836.
Chen Z, Han Y, Gu Y, et al. (2013): Cd11chighCD8+ regulatory T cell feedbach inhibits CD4 T cell Immune response via Fas ligand – Fas pathway. J Immunol 190: 6145-6154.
Churlaud G, Pitoiset F, Jebbawi F, et al. (2015): Human and mouse CD8+CD25+FOXP3+ regulatory T cells at steady state during interleukin-2 therapy. Front Immunol 6: 1-10.
Akane K, Kojima S, Mak TW, et al. (2016): CD8+CD122+CD49dlow regulatory T cells maintain T-cell homeostasis by killing activated T cells via Fas/FasL-mediated cytotoxicity. Proc Natl Acad Sci USA 113: 2460-2465.
Liu J, Chen D, Nie GD, Dai Z (2015): CD8+CD122+ T-cells: a newly emerging regulator with central memory cell phenotypes. Front Immunol 6: 1-6.
Suzuki H, Shi Z, Okuno Y, Isobe K (2008): Are CD8+CD122+ cells regulatory T cells or memory T cells? Hum Immunol 69: 751-754.
Dai H, Wan N, Zhang S, et al. (2010): Cutting edge: programmed death-1 defines CD8+CD122+ T cells as regulatory versus memory T cells. J Immunol 185: 803-807.
Li S, Xie Q, Zeng Y, et al. (2014): A naturally occurring CD8+CD122+ T-cell subset as a memory-like Treg family. Cell Mol Immunol 11: 326-331.
Gratz IK, Truong HA, Yang SH, et al. (2013): Cutting edge: memory regulatory T cells require IL-7 and not IL-2 for their maintenance in peripheral tissues. J Immunol 190: 4483-4487.
Sanchez Rodriguez R, Pauli ML, Neuhaus IM, et al. (2014): Memory regulatory T cells reside in human skin. J Clin Invest 124: 1027-1036.
Vukmanovic-Stejic M, Zhang Y, Cook JE, et al. (2006): Human CD4+CD25hiFoxp3+ regulatory T cells are derived by rapid turnover of memory populations in vivo. J Clin Invest 116: 2423-2433.
Guo Z, Jang MH, Otani K, et al. (2008): CD4+CD25+ regulatory T cells in the small intestinal lamina propria show an effector/memory phenotype. Int Immunol 20: 307-315.
Sanchez AM, Zhu J, Huang X, Yang Y (2012): The development and function of memory regulatory T cells after acute viral infections. J Immunol 189: 2805-2814.
Gratz IK, Campbell DJ (2014): Organ-specific and memory Treg cells: specifity, development, function and maintance. Front Immunol 5: 51-67.
Rosenblum MD, Way SS, Abbas AK (2016): Regulatory T cell memory. Nat Rev Immunol 16: 90-101.
Rowe JH, Ertelt JM, Xin L, Way SS (2012): Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 490: 102-106.
Kinder JM, Jiang TT, Clark DR, et al. (2014): Pregnancy – induced maternal regulatory T cells, bona fide memory or maintenance by antigenic reminder from fetal cell microchimerism? Chimerism 5: 16-19.
Ruocco MG, Chaouat G, Florez L, et al. (2014): Regulatory T-cells in pregnancy: historical perspective, state of the art, and burning questions. Front Immunol 5: 1-10.
Tsiantoulas D, Diehl CJ, Witztum JL, Binder CJ (2014): B cells and humoral immunity in atherosclerosis. Circ Res 114: 1743-1756.
Zasada M, Rutkowska-Zapała M, Lenart M, Kwinta P (2016): Rola limfocytów IRA B w wybranych procesach zapalnych. Post Hig Med Dosw 70: 164-199.
Rosser EC, Mauri C (2015): Regulatory B cells: origin, phenotype, and function. Immunity 42: 607-612.
Mauri C, Menon M (2015): The expanding family of regulatory B cells. Int Immunol 27: 479-486.
Sattler S, van der Vlugt LEPM, Hussaarts L: Regulatory B cells - implications in autoimmune and allergic disorders. In: Recent Advances in Immunology to Target Cancer, Inflammation and Infections, Kanwar JR (eds.). InTech 2012: 177-200.
Guzman-Genuino RM, Diener KR (2017): Regulatory B cells in pregnancy: lessons from autoimmunity, graft tolerance, and cancer. Front Immunol 8: 172.
Dörner T, Radbruch A (2007): Antibodies and B cell memory in viral immunity. Immunity 27: 384-392.
Kurosaki T, Kometani K, Ise W (2015): Memory B cells. Nat Rev Immunology 15: 149-159.
Tangye SG, Tarlinton DM (2009): Memory B cells: Effectors of long-lived immune responses. Eur J Immunol 39: 2065-2075.
Qi H (2016): T follicular helper cells in space-time. Nat Rev Immunol 16: 612-625.
Baumgarth N (2016): B-1 cell heterogeneity and the regulation of natural and antigen-induced IgM production. Front Immunol 7: 1-9.
Born WK, Huang Y, Zeng W, et al. (2016): A special connection between T cells and natural antibodies? Arch Imunol Ther Exp 64: 455-462.
Rothstein TL (2016): Natural antibodies as rheostats for susceptibility to chronic diseases in the aged. Front Immunol 7: 1-7.
Savage HP, Baumgarth N (2015): Characteristics of natural antibody – secreting cells. Ann N.Y. Acad Sci 1362: 132-142.
Zan H, Casali P (2015): Epigenetics of peripheral B-cell differentiation and the antibody response. Front Immunol 6: 631.
Bar-Or A, Oliveira EML, Anderson DE, et al. (2001): Immunological memory: Contribution of memory B cells expressing costimulatory molecules in the resting state. J Immunol 167: 5669-5677.
Stone SL, Lund FE (2016): IgM memory cells: first responders in malaria. Immunity 45: 235-237.
Lindner C, Thomsen I, Wahl B, et al. (2015): Diversification of memory B cells drives the continuous adaptation of secretory antibodies to gut microbiota. Nat Immunol 16: 880-888.
Onodera T, Takahashi Y, Yokoi Y, et al. (2012): Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc Natl Acad Sci USA 109: 2485-2490.
Li H, Borrego F, Nagata S, Tolnaz M (2016): Fc receptor-like 5 expression distinguishes two distinct subsets of human circulating tissue-like memory B cells. J Immunol 196: 4064-4074.
Barrington RA, Pozdnyakova O, Zafari MR, et al. (2002): B lymphocyte memory: Role of stromal cell complement and FcRIIB receptors. J Exp Med 196: 1189-1199.
Lazarevic V, Glimcher LH, Lord GM (2013): T-bet: a bridge between innate and adaptive immunity. Nat Rev Immunol 13: 777-789.
Geiger TL, Sun JC (2016): Development and maturation of natural killer cells. Curr Opin Immunol 39: 82-89.
Vivier E, Raulet DH, Moretta A, et al. (2011): Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
Vivier E, Tomasello E, Bartin M, et al. (2008): Functions of natural killer cells. Nat Immunol 9: 503-510.
Niedźwiedzka-Rystwej P, Herberg M, Deptuła W (2012): Biology and role of NK cells selected data. Centr Eur J Immunol 37: 399-404.
Moretta L, Montaldo E, Vacca P, et al. (2014): Human Natural Killer cells: origin, receptors, function, and clinical application. Int Arch. Allergy Immunol 164: 253-264.
Della Chiesa M, Pesce S, Muccio L, et al. (2016): Features of Memory-Like and PD-1+ human NK cells subsets. Front Immunol 7: 1-8.
Björkström NK, Ljunggren HG, Michaëlsson J (2016): Emerging insights into natural killer cells in human peripheral tissues. Nat Rev Immunol 16: 310-320.
Marcus A, Raulet DH (2013): Evidence for natural killer cell memory. Curr Biol 23: R817-820.
O’Sullivan TE, Sun JC, Lanier LL (2015): Natural killer cell memory. Immunity 43: 634-645.
Gardiner CM, Mills KHG (2016): The cells that mediate innate immune memory and their functional significance in inflammatory and infectious disease. Semin Immunol 28: 343-350.
O’Leary JG, Goodarzi M, Drayton DL, von Andrian UH (2006): T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7: 507-516.
Watzl C, Urlaub D, Fasenbender F, Claus M (2014): Natural killer cell regulation – beyond the receptors. F1000Prime Rep 6: 87.
Cerwenka A, Lanier LL (2016): Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol 16: 112-123.
Min-Oo G, Kamimura Y, Hendricks DW, et al. (2013): Natural killer cells: walking three paths down memory lane. Trends Immunol 34: 251-258.
Sun JC, Beike JN, Lanier LL (2009): Adaptive immune features of natural killer cells. Nature 457: 557-561.
Hamon MA, Quintin J (2016): Innate immune memory in mammals. Semin Immunol 28: 351-358.
Holmes TD, Bryceson YT (2016): Natural killer cell memory in context. Semin Immunol 28: 368-376.
Sun JC, Beike JN, Lanier LL (2010): Immune memory redefined: characterizing the longevity of natural killer cells. Immunol Rev 236: 83-94.
Sun JC, Lopez-Verges S, Kim CC, et al. (2011): NK cells and immune „memory”. J Immunol 186: 1891-1897.
Paust S, Gill HS, Wang BZ, et al. (2010): Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol 11: 1127-1135.
Paust S, von Andrian UH (2011): Natural killer cell memory. Nat Immunol 12: 500-508.
Fu X, Liu Y, Li L, et al. (2011): Human natural killer cells expressing the memory – associated marker CD45RO from tuberculous pleurisy respond more strongly and rapidly than CD45RO- natural killer cells following stimulation with interleukin-12. Immunology 134: 42-49.
Cooper MA, Elliot JM, Keyel PA, et al. (2009): Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 106: 1915-1919.
Rölle A, Pollmann J, Cerwenka A (2013): Memory of infections: an emerging role for natural killer cells. PLoS Pathog 9: e1003548.
Quick links
© 2019 Termedia Sp. z o.o. All rights reserved.
Developed by Bentus.
PayU - płatności internetowe