The role of myeloid-derived suppressor cells in immune ontogeny

Frontiers in Immunology

Volumn 5, Issue AUG, 2014, Pages

  Gantt, Soren ^a   Gervassi, Ana ^b   Jaspan, Heather ^b,c   Horton, Helen ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Seattle BioMed ^*  (Belgium)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Feto maternal tolerance; Immune ontogeny; Myeloid derived suppressor cells; Neonate

Indexed keywords

ARGINASE 1; ARGININE; B7 ANTIGEN; CD11B ANTIGEN; CD14 ANTIGEN; CD15 ANTIGEN; CD16 ANTIGEN; CD3 ANTIGEN; CD33 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CYCLIN D3; CYCLIN DEPENDENT KINASE 4; CYCLOOXYGENASE 2; ECALECTIN; GAMMA INTERFERON; HEME OXYGENASE 1; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; LYMPHOCYTE ANTIGEN; NATURAL KILLER CELL RECEPTOR NKG2D; NITRIC OXIDE SYNTHASE; ORNITHINE; PROGRAMMED DEATH 1 LIGAND 1; PROSTAGLANDIN E2; STEM CELL FACTOR; UNINDEXED DRUG; VASCULOTROPIN;

ABORTION; ADAPTIVE IMMUNITY; BONE MARROW CELL; CELL ACTIVATION; CELL PROLIFERATION; CYTOTOXICITY; DENDRITIC CELL; GRANULOCYTE; HUMAN; IMMUNITY; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NONHUMAN; ONTOGENY; PHENOTYPE; PREMATURITY; REGULATORY T LYMPHOCYTE; REVIEW; STEM CELL TRANSPLANTATION; SUPPRESSOR CELL; UMBILICAL CORD BLOOD;

EID: 84929078863     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00387     Document Type: Review

References (91)

1. Blencowe H, Cousens S. Addressing the challenge of neonatal mortality. Trop Med Int Health (2013) 18:303-12. doi:10.1111/tmi.12048
2. Wilson CB, Lewis DB. Basis and implications of selectively diminished cytokine production in neonatal susceptibility to infection. Rev Infect Dis (1990) 12(Suppl 4):S410-20. doi:10.1093/clinids/12.Supplement_4.S410
3. Kovarik J, Siegrist CA. Immunity in early life. Immunol Today (1998) 19:150-2. doi:10.1016/S0167-5699(97)01230-9
4. Levy O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol (2007) 7:379-90. doi:10.1038/nri2075
5. Philbin VJ, Levy O. Developmental biology of the innate immune response: implications for neonatal and infant vaccine development. Pediatr Res (2009) 65:98R-105R. doi:10.1203/PDR.0b013e31819f195d
6. Prendergast AJ, Klenerman P, Goulder PJ. The impact of differential antiviral immunity in children and adults. Nat Rev Immunol (2012) 12:636-48. doi:10.1038/nri3277
7. Makrigiannakis A, Karamouti M, Drakakis P, Loutradis D, Antsaklis A. Fetomaternal immunotolerance. Am J Reprod Immunol (2008) 60:482-96. doi:10.1111/j.1600-0897.2008.00655.x
8. Erlebacher A. Immunology of the maternal-fetal interface. Annu Rev Immunol (2013) 31:387-411. doi:10.1146/annurev-immunol-032712-100003
9. Kollmann TR, Levy O, Montgomery RR, Goriely S. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity (2012) 37:771-83. doi:10.1016/j.immuni.2012.10.014
10. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol (2009) 9:162-74. doi:10.1038/nri2506
11. Goh C, Narayanan S, Hahn YS. Myeloid-derived suppressor cells: the dark knight or the joker in viral infections? Immunol Rev (2013) 255:210-21. doi:10.1111/imr.12084
12. Albeituni SH, Ding C, Yan J. Hampering immune suppressors: therapeutic targeting of myeloid-derived suppressor cells in cancer. Cancer J (2013) 19:490-501. doi:10.1097/PPO.0000000000000006
13. Serafini P. Myeloid derived suppressor cells in physiological and pathological conditions: the good, the bad, and the ugly. Immunol Res (2013) 57:172-84. doi:10.1007/s12026-013-8455-2
14. Najjar YG, Finke JH. Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer. Front Oncol (2013) 3:49. doi:10.3389/fonc.2013.00049
15. Diaz-Montero CM, Finke J, Montero AJ. Myeloid-derived suppressor cells in cancer: therapeutic, predictive, and prognostic implications. Semin Oncol (2014) 41:174-84. doi:10.1053/j.seminoncol.2014.02.003
16. Strober S, Okada S, Oseroff A. Role of natural suppressor cells in allograft tolerance. Fed Proc (1984) 43:263-5.
17. Buessow SC, Paul RD, Lopez DM. Influence of mammary tumor progression on phenotype and function of spleen and in situ lymphocytes in mice. J Natl Cancer Inst (1984) 73:249-55.
18. Young MR, Endicott RA, Duffie GP, Wepsic HT. Suppressor alveolar macrophages in mice bearing metastatic Lewis lung carcinoma tumors. J Leukoc Biol (1987) 42:682-8.
19. Solito S, Falisi E, Diaz-Montero CM, Doni A, Pinton L, Rosato A, et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood (2011) 118:2254-65. doi:10.1182/blood-2010-12-325753
20. Qin A, Cai W, Pan T, Wu K, Yang Q, Wang N, et al. Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J Virol (2013) 87:1477-90. doi:10.1128/JVI.01759-12
21. Vollbrecht T, Stirner R, Tufman A, Roider J, Huber RM, Bogner JR, et al. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS (2012) 26:F31-7. doi:10.1097/QAD.0b013e328354b43f
22. du Plessis N, Loebenberg L, Kriel M, von Groote-Bidlingmaier F, Ribechini E, Loxton AG, et al. Increased frequency of myeloid-derived suppressor cells during active tuberculosis and after recent mycobacterium tuberculosis infection suppresses T-cell function. Am J Respir Crit Care Med (2013) 188:724-32. doi:10.1164/rccm.201302-0249OC
23. Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, et al. The terminology issue for myeloid-derived suppressor cells. Cancer Res (2007) 67:425. doi:10.1158/0008-5472.CAN-06-3037
24. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S, et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol (2010) 22:238-44. doi:10.1016/j.coi.2010.01.021
25. Pillay J, Tak T, Kamp VM, Koenderman L. Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell Mol Life Sci (2013) 70:3813-27. doi:10.1007/s00018-013-1286-4
26. Popovic PJ, Zeh HJ III, Ochoa JB. Arginine and immunity. J Nutr (2007) 137:1681S-6S.
27. Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, Piazuelo MB, et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res (2004) 64:5839-49. doi:10.1158/0008-5472.CAN-04-0465
28. Rodriguez PC, Quiceno DG, Ochoa AC. l-arginine availability regulates T-lymphocyte cell-cycle progression. Blood (2007) 109:1568-73. doi:10.1182/blood-2006-06-031856
29. Taheri F, Ochoa JB, Faghiri Z, Culotta K, Park HJ, Lan MS, et al. l-Arginine regulates the expression of the T-cell receptor zeta chain (CD3zeta) in Jurkat cells. Clin Cancer Res (2001) 7:958s-65s.
30. Baniyash M. TCR zeta-chain downregulation: curtailing an excessive inflammatory immune response. Nat Rev Immunol (2004) 4:675-87. doi:10.1038/nri1434
31. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, et al. Fas-induced caspase denitrosylation. Science (1999) 284:651-4. doi:10.1126/science.284.5414.651
32. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol (1998) 160:5729-34.
33. Harari O, Liao JK. Inhibition of MHC II gene transcription by nitric oxide and antioxidants. Curr Pharm Des (2004) 10:893-8. doi:10.2174/1381612043452893
34. Rivoltini L, Carrabba M, Huber V, Castelli C, Novellino L, Dalerba P, et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev (2002) 188:97-113. doi:10.1034/j.1600-065X.2002.18809.x
35. Condamine T, Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol (2011) 32:19-25. doi:10.1016/j.it.2010.10.002
36. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res (2010) 70:68-77. doi:10.1158/0008-5472.CAN-09-2587
37. Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol (2009) 182:240-9. doi:10.4049/jimmunol.182.1.240
38. Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood (2007) 109:4336-42. doi:10.1182/blood-2006-09-046201
39. Oberlies J, Watzl C, Giese T, Luckner C, Kropf P, Muller I, et al. Regulation of NK cell function by human granulocyte arginase. J Immunol (2009) 182:5259-67. doi:10.4049/jimmunol.0803523
40. Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P, et al. PD-L1 is a novel direct target of HIF-1a, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med (2014) 211:781-90. doi:10.1084/jem.20131916
41. De Wilde V, Van Rompaey N, Hill M, Lebrun JF, Lemaitre P, Lhomme F, et al. Endotoxin-induced myeloid-derived suppressor cells inhibit alloimmune responses via heme oxygenase-1. Am J Transplant (2009) 9:2034-47. doi:10.1111/j.1600-6143.2009.02757.x
42. Sumida K, Wakita D, Narita Y, Masuko K, Terada S, Watanabe K, et al. Anti-IL-6 receptor mAb eliminates myeloid-derived suppressor cells and inhibits tumor growth by enhancing T-cell responses. Eur J Immunol (2012) 42:2060-72. doi:10.1002/eji.201142335
43. Dugast AS, Haudebourg T, Coulon F, Heslan M, Haspot F, Poirier N, et al. Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion. J Immunol (2008) 180:7898-906. doi:10.4049/jimmunol.180.12.7898
44. Serafini P, Mgebroff S, Noonan K, Borrello I. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res (2008) 68:5439-49. doi:10.1158/0008-5472.CAN-07-6621
45. Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res (2006) 66:1123-31. doi:10.1158/0008-5472.CAN-05-1299
46. Hoechst B, Ormandy LA, Ballmaier M, Lehner F, Kruger C, Manns MP, et al. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology (2008) 135:234-43. doi:10.1053/j.gastro.2008.03.020
47. Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol (2007) 179:977-83. doi:10.4049/jimmunol.179.2.977
48. Van Rompaey N, Le Moine A. Myeloid-derived suppressor cells: characterization and expansion in models of endotoxemia and transplantation. Methods Mol Biol (2011) 677:169-80. doi:10.1007/978-1-60761-869-0_12
49. Arocena AR, Onofrio LI, Pellegrini AV, Carrera Silva AE, Paroli A, Cano RC, et al. Myeloid-derived suppressor cells are key players in the resolution of inflammation during a model of acute infection. Eur J Immunol (2014) 44:184-94. doi:10.1002/eji.201343606
50. Li RJ, Liu L, Gao W, Song XZ, Bai XJ, Li ZF. Cyclooxygenase-2 blockade inhibits accumulation and function of myeloid-derived suppressor cells and restores T cell response after traumatic stress. Journal of Huazhong University of Science and Technology (2014) 34:234-40. doi:10.1007/s11596-014-1264-6
51. Cuenca AG, Delano MJ, Kelly-Scumpia KM, Moreno C, Scumpia PO, Laface DM, et al. A paradoxical role for myeloid-derived suppressor cells in sepsis and trauma. Mol Med (2011) 17:281-92. doi:10.2119/molmed.2010.00178
52. Norris BA, Uebelhoer LS, Nakaya HI, Price AA, Grakoui A, Pulendran B. Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity (2013) 38:309-21. doi:10.1016/j.immuni.2012.10.022
53. Enioutina EY, Bareyan D, Daynes RA. A role for immature myeloid cells in immune senescence. J Immunol (2011) 186:697-707. doi:10.4049/jimmunol.1002987
54. Verschoor CP, Johnstone J, Millar J, Dorrington MG, Habibagahi M, Lelic A, et al. Blood CD33(+)HLA-DR(-) myeloid-derived suppressor cells are increased with age and a history of cancer. J Leukoc Biol (2013) 93:633-7. doi:10.1189/jlb.0912461
55. Kusmartsev S, Su Z, Heiser A, Dannull J, Eruslanov E, Kubler H, et al. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res (2008) 14:8270-8. doi:10.1158/1078-0432.CCR-08-0165
56. Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, et al. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res (2006) 66:9299-307. doi:10.1158/0008-5472.CAN-06-1690
57. Lathers DM, Clark JI, Achille NJ, Young MR. Phase 1B study to improve immune responses in head and neck cancer patients using escalating doses of 25-hydroxyvitamin D3. Cancer Immunol Immunother (2004) 53:422-30. doi:10.1007/s00262-003-0459-7
58. Ugel S, Delpozzo F, Desantis G, Papalini F, Simonato F, Sonda N, et al. Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol (2009) 9:470-81. doi:10.1016/j.coph.2009.06.014
59. Dowling DJ, Levy O. Ontogeny of early life immunity. Trends Immunol (2014) 35:299-310. doi:10.1016/j.it.2014.04.007
60. Elahi S, Ertelt JM, Kinder JM, Jiang TT, Zhang X, Xin L, et al. Immunosuppressive CD71+ erythroid cells compromise neonatal host defence against infection. Nature (2013) 504:158-62. doi:10.1038/nature12675
61. Siegrist CA. Neonatal and early life vaccinology. Vaccine (2001) 19:3331-46. doi:10.1016/S0264-410X(01)00028-7
62. Yabuhara A, Kawai H, Komiyama A. Development of natural killer cytotoxicity during childhood: marked increases in number of natural killer cells with adequate cytotoxic abilities during infancy to early childhood. Pediatr Res (1990) 28:316-22. doi:10.1203/00006450-199010000-00002
63. Dominguez E, Madrigal JA, Layrisse Z, Cohen SB. Fetal natural killer cell function is suppressed. Immunology (1998) 94:109-14. doi:10.1046/j.1365-2567.1998.00489.x
64. Kenzel S, Henneke P. The innate immune system and its relevance to neonatal sepsis. Curr Opin Infect Dis (2006) 19:264-70. doi:10.1097/01.qco.0000224821.27482.bd
65. Kollmann TR, Crabtree J, Rein-Weston A, Blimkie D, Thommai F, Wang XY, et al. Neonatal innate TLR-mediated responses are distinct from those of adults. J Immunol (2009) 183:7150-60. doi:10.4049/jimmunol.0901481
66. Jacobson A, Bell F, Lejarcegui N, Mitchell C, Frenkel L, Horton H. Healthy Neonates Possess a CD56-Negative NK Cell Population with Reduced Anti-Viral Activity. PLoS One (2013) 8:e67700. doi:10.1371/journal.pone.0067700
67. Bertotto A, Gerli R, Lanfrancone L, Crupi S, Arcangeli C, Cernetti C, et al. Activation of cord T lymphocytes. II. Cellular and molecular analysis of the defective response induced by anti-CD3 monoclonal antibody. Cell Immunol (1990) 127:247-59. doi:10.1016/0008-8749(90)90130-J
68. Pirenne-Ansart H, Paillard F, De Groote D, Eljaafari A, Le Gac S, Blot P, et al. Defective cytokine expression but adult-type T-cell receptor, CD8, and p56lck modulation in CD3- or CD2-activated T cells from neonates. Pediatr Res (1995) 37:64-9. doi:10.1203/00006450-199501000-00013
69. Wu CY, Demeure C, Kiniwa M, Gately M, Delespesse G. IL-12 induces the production of IFN-gamma by neonatal human CD4 T cells. J Immunol (1993) 151:1938-49.
70. Burchett SK, Corey L, Mohan KM, Westall J, Ashley R, Wilson CB. Diminished interferon-gamma and lymphocyte proliferation in neonatal and postpartum primary herpes simplex virus infection. J Infect Dis (1992) 165:813-8. doi:10.1093/infdis/165.5.813
71. Zaghouani H, Hoeman CM, Adkins B. Neonatal immunity: faulty T-helpers and the shortcomings of dendritic cells. Trends Immunol (2009) 30:585-91. doi:10.1016/j.it.2009.09.002
72. Smith NL, Wissink E, Wang J, Pinello JF, Davenport MP, Grimson A, et al. Rapid Proliferation and Differentiation Impairs the Development of Memory CD8+ T Cells in Early Life. J Immunol (2014) 193:177-84. doi:10.4049/jimmunol.1400553
73. Mold JE, Michaëlsson J, Burt TD, Muench MO, Beckerman KP, Busch MP, et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science (2008) 322:1562-5. doi:10.1126/science.1164511
74. Gervassi A, Horton H. Is infant immunity actively suppressed or immature? Virology (2014) 2014:1-9. doi:10.4137/VRT.S12248
75. Rieber N, Gille C, Kostlin N, Schafer I, Spring B, Ost M, et al. Neutrophilic myeloid-derived suppressor cells in cord blood modulate innate and adaptive immune responses. Clin Exp Immunol (2013) 174:45-52. doi:10.1111/cei.12143
76. Gervassi A, Lejarcegui N, Dross S, Jacobson A, Gantt S, Jaspan H, et al. Early Life Immunity and Ability to Respond to Vaccines Hindered by Myeloid Derived Suppressor Cells: Implications for Infant HIV Vaccinology. Barcelona: AIDS Vaccine Mary Ann Liebert, Inc (2013). p. A152-3.
77. Gervassi A, Lejarcegui N, Dross S, Jacobson A, Itaya G, Kidzeru E, et al. Myeloid derived suppressor cells are present at high frequency in neonates and suppress in vitro T cell responses PLoS ONE (in press).
78. Angelone DF, Wessels MR, Coughlin M, Suter EE, Valentini P, Kalish LA, et al. Innate immunity of the human newborn is polarized toward a high ratio of IL-6/TNF-alpha production in vitro and in vivo. Pediatr Res (2006) 60:205-9. doi:10.1203/01.pdr.0000228319.10481.ea
79. Marodi L. Innate cellular immune responses in newborns. Clin Immunol (2006) 118:137-44. doi:10.1016/j.clim.2005.10.012
80. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol (2004) 5:266-71. doi:10.1038/ni1037
81. Michaelsson J, Mold JE, McCune JM, Nixon DF. Regulation of T cell responses in the developing human fetus. J Immunol (2006) 176:5741-8. doi:10.4049/jimmunol.176.10.5741
82. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature (2012) 490:102-6. doi:10.1038/nature11462
83. Mauti LA, Le Bitoux MA, Baumer K, Stehle JC, Golshayan D, Provero P, et al. Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J Clin Invest (2011) 121:2794-807. doi:10.1172/JCI41936
84. Spallanzani RG, Dalotto-Moreno T, Raffo Iraolagoitia XL, Ziblat A, Domaica CI, Avila DE, et al. Expansion of CD11b(+)Ly6G (+)Ly6C (int) cells driven by medroxyprogesterone acetate in mice bearing breast tumors restrains NK cell effector functions. Cancer Immunol Immunother (2013) 62:1781-95. doi:10.1007/s00262-013-1483-x
85. Chabtini L, Mfarrej B, Mounayar M, Zhu B, Batal I, Dakle PJ, et al. TIM-3 regulates innate immune cells to induce fetomaternal tolerance. J Immunol (2013) 190:88-96. doi:10.4049/jimmunol.1202176
86. Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM, et al. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol (2007) 37:935-45. doi:10.1002/eji.200636542
87. Köstlin N, Kugel H, Spring B, Leiber A, Marmé A, Henes M, et al. Granulocytic myeloid derived suppressor cells expand in human pregnancy and modulate T-cell responses. Eur J Immunol (2014). doi:10.1002/eji.201344200
88. Klemm RD, Labrique AB, Christian P, Rashid M, Shamim AA, Katz J, et al. Newborn vitamin A supplementation reduced infant mortality in rural Bangladesh. Pediatrics (2008) 122:e242-50. doi:10.1542/peds.2007-3448
89. Awasthi S, Peto R, Read S, Clark S, Pande V, Bundy D, et al. Vitamin A supplementation every 6 months with retinol in 1 million pre-school children in north India: DEVTA, a cluster-randomised trial. Lancet (2013) 381:1469-77. doi:10.1016/S0140-6736(12)62126-6
90. Rocha V, Wagner JE Jr., Sobocinski KA, Klein JP, Zhang MJ, Horowitz MM, et al. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. Eurocord and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N Engl J Med (2000) 342:1846-54. doi:10.1056/NEJM200006223422501
91. Trellakis S, Bruderek K, Hutte J, Elian M, Hoffmann TK, Lang S, et al. Granulocytic myeloid-derived suppressor cells are cryosensitive and their frequency does not correlate with serum concentrations of colony-stimulating factors in head and neck cancer. Innate Immun (2013) 19:328-36. doi:10.1177/1753425912463618