Pretreatment levels of circulating Th1 and Th2 cytokines, and their ratios, are associated with ER-negative and triple negative breast cancers

Breast Cancer Research and Treatment

Volumn 139, Issue 2, 2013, Pages 477-488

  Hong, Chi Chen ^a   Yao, Song ^a   McCann, Susan E ^a   Dolnick, Ree Y ^a   Wallace, Paul K ^a   Gong, Zhihong ^a   Quan, Lei ^a   Lee, Kelvin P ^a   Evans, Sharon S ^a   Repasky, Elizabeth A ^a   Edge, Stephen B ^a   Ambrosone, Christine B ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Cytokines; Estrogen negative breast cancer; Immune function; Triple negative breast cancer

Indexed keywords

ALPHA2 INTERFERON; CYTOKINE; EOTAXIN; ESTROGEN RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 3; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ARTICLE; BLOOD LEVEL; BREAST CANCER; CELL ASSAY; CELL TYPE; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ESTROGEN RECEPTOR NEGATIVE BREAST CANCER; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMORAL IMMUNITY; MAJOR CLINICAL STUDY; MOLECULAR DYNAMICS; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TH1 CELL; TH1 TH2 BALANCE; TH2 CELL; TISSUE CHARACTERIZATION; TRIPLE NEGATIVE BREAST CANCER;

ADULT; AGED; AGED, 80 AND OVER; BREAST NEOPLASMS; CYTOKINES; FEMALE; HUMANS; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; RECEPTORS, ESTROGEN; TH1 CELLS; TH2 CELLS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84878746618     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-013-2549-3     Document Type: Article

References (107)

1. Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492-2502. doi: 10.1001/jama.295.21.2492
2. Blows FM, Driver KE, Schmidt MK et al (2010) Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies. PLoS Med 7:e1000279. doi: 10.1371/journal.pmed.1000279
3. Tischkowitz M, Brunet JS, Begin LR et al (2007) Use of immunohistochemical markers can refine prognosis in triple negative breast cancer. BMC Cancer 7:134. doi: 10.1186/1471-2407-7-134
4. Nofech-Mozes S, Trudeau M, Kahn HK et al (2009) Patterns of recurrence in the basal and non-basal subtypes of triple-negative breast cancers. Breast Cancer Res Treat 118:131-137. doi: 10.1007/s10549-008-0295-8
5. Carey L, Winer E, Viale G et al (2010) Triple-negative breast cancer: disease entity or title of convenience? Nat Rev Clin Oncol 7:683-692. doi: 10.1038/nrclinonc.2010.154
6. Millikan RC, Newman B, Tse CK et al (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123-139. doi: 10.1007/s10549-007- 9632-6
7. Hines LM, Risendal B, Byers T et al (2011) Ethnic disparities in breast tumor phenotypic subtypes in Hispanic and non-Hispanic white women. J Womens Health (Larchmt) 20:1543-1550. doi: 10.1089/jwh.2010.2558
8. Davis AA, Kaklamani VG (2012) Metabolic syndrome and triple-negative breast cancer: a new paradigm. Int J Breast Cancer 2012:809291. doi: 10.1155/2012/809291
9. Kwan ML, Kushi LH, Weltzien E et al (2009) Epidemiology of breast cancer subtypes in two prospective cohort studies of breast cancer survivors. Breast Cancer Res 11:R31. doi: 10.1186/bcr2261
10. Pierce BL, Ballard-Barbash R, Bernstein L et al (2009) Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol 27:3437-3444. doi: 10.1200/JCO.2008.18.9068
11. Benoy IH, Salgado R, Van Dam P et al (2004) Increased serum interleukin-8 in patients with early and metastatic breast cancer correlates with early dissemination and survival. Clin Cancer Res 10:7157-7162. doi: 10.1158/1078-0432.CCR-04-0812
12. Teschendorff AE, Miremadi A, Pinder SE et al (2007) An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 8:R157. doi: 10.1186/gb-2007-8-8-r157
13. Rody A, Karn T, Liedtke C et al (2011) A clinically relevant gene signature in triple negative and basal-like breast cancer. Breast Cancer Res 13:R97. doi: 10.1186/bcr3035
14. Bianchini G, Qi Y, Alvarez RH et al (2010) Molecular anatomy of breast cancer stroma and its prognostic value in estrogen receptor-positive and -negative cancers. J Clin Oncol 28:4316-4323. doi: 10.1200/JCO.2009.27.2419
15. DeNardo DG, Coussens LM (2007) Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res 9:212. doi: 10.1186/bcr1746
16. Bindea G, Mlecnik B, Fridman WH et al (2010) Natural immunity to cancer in humans. Curr Opin Immunol 22:215-222. doi: 10.1016/j.coi.2010.02.006
17. Pardoll D (2009) Metastasis-promoting immunity: when T cells turn to the dark side. Cancer Cell 16:81-82. doi: 10.1016/j.ccr.2009.07.007
18. Waugh DJ, Wilson C (2008) The interleukin-8 pathway in cancer. Clin Cancer Res 14:6735-6741. doi: 10.1158/1078-0432.CCR-07-4843
19. Gabay C (2006) Interleukin-6 and chronic inflammation. Arthritis Res Ther 8(Suppl 2):S3. doi: 10.1186/ar1917
20. Salgado R, Junius S, Benoy I et al (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 103:642-646. doi: 10.1002/ijc.10833
21. Elenkov IJ (2004) Glucocorticoids and the Th1/Th2 balance. Ann N Y Acad Sci 1024:138-146. doi: 10.1196/annals.1321.010
22. Kidd P (2003) Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev 8:223-246
23. Onoe K, Yanagawa Y, Minami K et al (2007) Th1 or Th2 balance regulated by interaction between dendritic cells and NKT cells. Immunol Res 38:319-332
24. Ambrosone CB, Nesline MK, Davis W (2006) Establishing a cancer center data bank and biorepository for multidisciplinary research. Cancer Epidemiol Biomarkers Prev 15:1575-1577
25. Yao S, Sucheston LE, Millen AE et al (2011) Pretreatment serum concentrations of 25-hydroxyvitamin D and breast cancer prognostic characteristics: a case-control and a case-series study. PLoS ONE 6:e17251. doi: 10.1371/journal.pone.0017251
26. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289-300
27. Laoui D, Movahedi K, Van Overmeire E et al (2011) Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol 55:861-867. doi: 10.1387/ijdb.113371dl
28. Sheu BC, Chang WC, Cheng CY et al (2008) Cytokine regulation networks in the cancer microenvironment. Front Biosci 13:6255-6268
29. Wilson J, Balkwill F (2002) The role of cytokines in the epithelial cancer microenvironment. Semin Cancer Biol 12:113-120. doi: 10.1006/scbi.2001. 0419
30. Goldberg JE, Schwertfeger KL (2010) Proinflammatory cytokines in breast cancer: mechanisms of action and potential targets for therapeutics. Curr Drug Targets 11:1133-1146
31. Lyon DE, McCain NL, Walter J et al (2008) Cytokine comparisons between women with breast cancer and women with a negative breast biopsy. Nurs Res 57:51-58
32. Saglam S, Suzme R, Gurdol F (2009) Serum tumor necrosis factor-alpha and interleukin-2 concentrations in newly diagnosed ERBB2 (HER2/neu) positive breast cancer patients. Int J Biol Markers 24:142-146
33. Gonzalez RM, Daly DS, Tan R et al (2011) Plasma biomarker profiles differ depending on breast cancer subtype but RANTES is consistently increased. Cancer Epidemiol Biomarkers Prev 20:1543-1551. doi: 10.1158/1055-9965.EPI-10-1248
34. Narita D, Seclaman E, Ursoniu S et al (2011) Expression of CCL18 and interleukin-6 in the plasma of breast cancer patients as compared with benign tumor patients and healthy controls. Rom J Morphol Embryol 52:1261-1267
35. Pusztai L, Mendoza TR, Reuben JM et al (2004) Changes in plasma levels of inflammatory cytokines in response to paclitaxel chemotherapy. Cytokine 25:94-102
36. Herrera AC, Panis C, Victorino VJ, Campos FC, Colado-Simão AN, Cecchini AL, Cecchini R (2012) Molecular subtype is determinant on inflammatory status and immunological profile from invasive breast cancer patients. Cancer Immunol Immunother 61(11):2193-2201. doi: 10.1007/s00262-012-1283-8
37. Corren J (2012) Inhibition of interleukin-5 for the treatment of eosinophilic diseases. Discov Med 13:305-312
38. Corren J (2011) Anti-interleukin-5 antibody therapy in asthma and allergies. Curr Opin Allergy Clin Immunol 11:565-570. doi: 10.1097/ACI. 0b013e32834c3d30
39. Lee JJ, Jacobsen EA, McGarry MP et al (2010) Eosinophils in health and disease: the LIAR hypothesis. Clin Exp Allergy 40:563-575. doi: 10.1111/j.1365-2222.2010.03484.x
40. Clutterbuck EJ, Hirst EM, Sanderson CJ (1989) Human interleukin-5 (IL-5) regulates the production of eosinophils in human bone marrow cultures: comparison and interaction with IL-1, IL-3, IL-6, and GMCSF. Blood 73:1504-1512
41. Till S, Dickason R, Huston D et al (1997) IL-5 secretion by allergen-stimulated CD4+ T cells in primary culture: relationship to expression of allergic disease. J Allergy Clin Immunol 99:563-569
42. Simson L, Foster PS (2000) Chemokine and cytokine cooperativity: eosinophil migration in the asthmatic response. Immunol Cell Biol 78:415-422. doi: 10.1046/j.1440-1711.2000.00922.x
43. Cai Y, Zhou J, Webb DC (2012) Estrogen stimulates Th2 cytokine production and regulates the compartmentalisation of eosinophils during allergen challenge in a mouse model of asthma. Int Arch Allergy Immunol 158:252-260. doi: 10.1159/000331437
44. Katz O, Sheiner E (2008) Asthma and pregnancy: a review of two decades. Expert Rev Respir Med 2:97-107. doi: 10.1586/17476348.2.1.97
45. Vojtechova P, Martin RM (2009) The association of atopic diseases with breast, prostate, and colorectal cancers: a meta-analysis. Cancer Causes Control 20:1091-1105. doi: 10.1007/s10552-009-9334-y
46. Moorman JE, Rudd RA, Johnson CA et al (2007) National surveillance for asthma - United States, 1980-2004. MMWR Surveill Summ 56:1-54
47. Holgate ST (2012) Innate and adaptive immune responses in asthma. Nat Med 18:673-683. doi: 10.1038/nm.2731
48. Oliphant CJ, Barlow JL, McKenzie AN (2011) Insights into the initiation of type 2 immune responses. Immunology 134:378-385. doi: 10.1111/j.1365-2567. 2011.03499.x
49. Anthony RM, Rutitzky LI, Urban JF Jr et al (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7:975-987. doi: 10.1038/nri2199
50. Rook GA (2009) Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126:3-11. doi: 10.1111/j.1365-2567.2008.03007.x
51. Lyons TR, Schedin PJ, Borges VF (2009) Pregnancy and breast cancer: when they collide. J Mammary Gland Biol Neoplasia 14:87-98. doi: 10.1007/s10911-009- 9119-7
52. O'Brien J, Lyons T, Monks J et al (2010) Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol 176:1241-1255. doi: 10.2353/ajpath.2010.090735
53. O'Brien J, Schedin P (2009) Macrophages in breast cancer: do involution macrophages account for the poor prognosis of pregnancy-associated breast cancer? J Mammary Gland Biol Neoplasia 14:145-157. doi: 10.1007/s10911-009-9118- 8
54. Reinhard G, Noll A, Schlebusch H et al (1998) Shifts in the TH1/TH2 balance during human pregnancy correlate with apoptotic changes. Biochem Biophys Res Commun 245:933-938. doi: 10.1006/bbrc.1998.8549
55. Saito S, Tsukaguchi N, Hasegawa T et al (1999) Distribution of Th1, Th2, and Th0 and the Th1/Th2 cell ratios in human peripheral and endometrial T cells. Am J Reprod Immunol 42:240-245
56. Saito S, Sakai M, Sasaki Y et al (1999) Quantitative analysis of peripheral blood Th0, Th1, Th2 and the Th1:Th2 cell ratio during normal human pregnancy and preeclampsia. Clin Exp Immunol 117:550-555
57. Sykes L, MacIntyre DA, Yap XJ et al (2012) Changes in the Th1:Th2 cytokine bias in pregnancy and the effects of the anti-inflammatory cyclopentenone prostaglandin 15-deoxy-Delta(12,14)-prostaglandin J2. Mediators Inflamm 2012:416739. doi: 10.1155/2012/416739
58. Luppi P (2003) How immune mechanisms are affected by pregnancy. Vaccine 21:3352-3357
59. Rastogi D, Wang C, Lendor C et al (2006) T-helper type 2 polarization among asthmatics during and following pregnancy. Clin Exp Allergy 36:892-898. doi: 10.1111/j.1365-2222.2006.02519.x
60. Halonen M, Lohman IC, Stern DA et al (2009) Th1/Th2 patterns and balance in cytokine production in the parents and infants of a large birth cohort. J Immunol 182:3285-3293. doi: 10.4049/jimmunol.0711996
61. Groer MW, Davis MW (2006) Cytokines, infections, stress, and dysphoric moods in breastfeeders and formula feeders. J Obstet Gynecol Neonatal Nurs 35:599-607. doi: 10.1111/j.1552-6909.2006.00083.x
62. Dimitrov S, Lange T, Fehm HL et al (2004) A regulatory role of prolactin, growth hormone, and corticosteroids for human T-cell production of cytokines. Brain Behav Immun 18:368-374. doi: 10.1016/j.bbi.2003.09.014
63. Meli R, Bentivoglio C, Nuzzo I et al (2003) Th1-Th2 response in hyperprolactinemic mice infected with Salmonella enterica serovar Typhimurium. Eur Cytokine Netw 14:186-191
64. Weiss JM, Subleski JJ, Wigginton JM et al (2007) Immunotherapy of cancer by IL-12-based cytokine combinations. Expert Opin Biol Ther 7:1705-1721. doi: 10.1517/14712598.7.11.1705
65. Duda DG, Sunamura M, Lozonschi L et al (2000) Direct in vitro evidence and in vivo analysis of the antiangiogenesis effects of interleukin 12. Cancer Res 60:1111-1116
66. Kozlowski L, Zakrzewska I, Tokajuk P et al (2003) Concentration of interleukin-6 (IL-6), interleukin-8 (IL-8) and interleukin-10 (IL-10) in blood serum of breast cancer patients. Rocz Akad Med Bialymst 48:82-84
67. Hussein MZ, Al Fikky A, Abdel Bar I et al (2004) Serum IL-6 and IL-12 levels in breast cancer patients. Egypt J Immunol 11:165-170
68. Critchley-Thorne RJ, Simons DL, Yan N et al (2009) Impaired interferon signaling is a common immune defect in human cancer. Proc Natl Acad Sci USA 106:9010-9015. doi: 10.1073/pnas.0901329106
69. Brassard DL, Grace MJ, Bordens RW (2002) Interferon-alpha as an immunotherapeutic protein. J Leukoc Biol 71:565-581
70. Biron CA (1998) Role of early cytokines, including alpha and beta interferons (IFN-alpha/beta), in innate and adaptive immune responses to viral infections. Semin Immunol 10:383-390. doi: 10.1006/smim.1998.0138
71. Wenner CA, Guler ML, Macatonia SE et al (1996) Roles of IFN-gamma and IFN-alpha in IL-12-induced T helper cell-1 development. J Immunol 156:1442-1447
72. Eguchi J, Hiroishi K, Ishii S et al (2003) Interferon-alpha and interleukin-12 gene therapy of cancer: interferon-alpha induces tumor-specific immune responses while interleukin-12 stimulates non-specific killing. Cancer Immunol Immunother 52:378-386. doi: 10.1007/s00262-002-0367-2
73. Moschos SJ, Edington HD, Land SR et al (2006) Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon alfa-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. J Clin Oncol 24:3164-3171. doi: 10.1200/JCO.2005.05. 2498
74. Bleotu C, Chifiriuc MC, Grigore R et al (2012) Investigation of Th1/Th2 cytokine profiles in patients with laryngo-pharyngeal. HPV-positive cancers. Eur Arch Otorhinolaryngol. doi: 10.1007/s00405-012-2067-7
75. Ubukata H, Motohashi G, Tabuchi T et al (2010) Evaluations of interferon-gamma/interleukin-4 ratio and neutrophil/lymphocyte ratio as prognostic indicators in gastric cancer patients. J Surg Oncol 102:742-747. doi: 10.1002/jso.21725
76. Crane IJ, Forrester JV (2005) Th1 and Th2 lymphocytes in autoimmune disease. Crit Rev Immunol 25:75-102
77. Ghoreschi K, Thomas P, Breit S et al (2003) Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease. Nat Med 9:40-46. doi: 10.1038/nm804
78. Nguyen TH, Casale TB (2011) Immune modulation for treatment of allergic disease. Immunol Rev 242:258-271. doi: 10.1111/j.1600-065X.2011.01034.x
79. Hamilton DH, Bretscher PA (2008) Different immune correlates associated with tumor progression and regression: implications for prevention and treatment of cancer. Cancer Immunol Immunother 57:1125-1136. doi: 10.1007/s00262-007- 0442-9
80. Kennedy R, Celis E (2008) Multiple roles for CD4+ T cells in anti-tumor immune responses. Immunol Rev 222:129-144. doi: 10.1111/j.1600-065X.2008.00616.x
81. DeNardo DG, Barreto JB, Andreu P et al (2009) CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16:91-102. doi: 10.1016/j.ccr.2009.06.018
82. Goodman WA, Levine AD, Massari JV et al (2009) IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J Immunol 183:3170-3176. doi: 10.4049/jimmunol.0803721
83. Oh SH, Park CO, Wu WH et al (2012) Corticotropin-releasing hormone downregulates IL-10 production by adaptive forkhead box protein 3-negative regulatory T cells in patients with atopic dermatitis. J Allergy Clin Immunol 129:151-9.e1-6. doi: 10.1016/j.jaci.2011.09.008
84. Chaudhry A, Samstein RM, Treuting P et al (2011) Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 34:566-578. doi: 10.1016/j.immuni.2011.03.018
85. Pace L, Pioli C, Doria G (2005) IL-4 modulation of CD4+ CD25+ T regulatory cell-mediated suppression. J Immunol 174:7645-7653
86. Gooch JL, Lee AV, Yee D (1998) Interleukin 4 inhibits growth and induces apoptosis in human breast cancer cells. Cancer Res 58:4199-4205
87. Toi M, Bicknell R, Harris AL (1992) Inhibition of colon and breast carcinoma cell growth by interleukin-4. Cancer Res 52:275-279
88. Gooch JL, Christy B, Yee D (2002) STAT6 mediates interleukin-4 growth inhibition in human breast cancer cells. Neoplasia 4:324-331. doi: 10.1038/sj.neo.7900248
89. Nagai S, Toi M (2000) Interleukin-4 and breast cancer. Breast Cancer 7:181-186
90. Hochrein H, O'Keeffe M, Luft T et al (2000) Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J Exp Med 192:823-833
91. Ebner S, Ratzinger G, Krosbacher B et al (2001) Production of IL-12 by human monocyte-derived dendritic cells is optimal when the stimulus is given at the onset of maturation, and is further enhanced by IL-4. J Immunol 166:633-641
92. Bream JH, Curiel RE, Yu CR et al (2003) IL-4 synergistically enhances both IL-2- and IL-12-induced IFN-gamma expression in murine NK cells. Blood 102:207-214. doi: 10.1182/blood-2002-08-2602
93. Eguchi J, Hiroishi K, Ishii S et al (2005) Interleukin-4 gene transduced tumor cells promote a potent tumor-specific Th1-type response in cooperation with interferon-alpha transduction. Gene Ther 12:733-741. doi: 10.1038/sj.gt.3302401
94. Chavey C, Bibeau F, Gourgou-Bourgade S et al (2007) Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res 9:R15. doi: 10.1186/bcr1648
95. Green AR, Green VL, White MC et al (1997) Expression of cytokine messenger RNA in normal and neoplastic human breast tissue: identification of interleukin-8 as a potential regulatory factor in breast tumours. Int J Cancer 72:937-941
96. Venetsanakos E, Beckman I, Bradley J et al (1997) High incidence of interleukin 10 mRNA but not interleukin 2 mRNA detected in human breast tumours. Br J Cancer 75:1826-1830
97. Freund A, Chauveau C, Brouillet JP et al (2003) IL-8 expression and its possible relationship with estrogen-receptor-negative status of breast cancer cells. Oncogene 22:256-265
98. Lin Y, Huang R, Chen L et al (2004) Identification of interleukin-8 as estrogen receptor-regulated factor involved in breast cancer invasion and angiogenesis by protein arrays. Int J Cancer 109:507-515. doi: 10.1002/ijc.11724
99. Soria G, Ofri-Shahak M, Haas I et al (2011) Inflammatory mediators in breast cancer: coordinated expression of TNFalpha & IL-1beta with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition. BMC Cancer 11:130. doi: 10.1186/1471-2407-11-130
100. Pantschenko AG, Pushkar I, Anderson KH et al (2003) The interleukin-1 family of cytokines and receptors in human breast cancer: implications for tumor progression. Int J Oncol 23:269-284
101. Singer CF, Hudelist G, Gschwantler-Kaulich D et al (2006) Interleukin-1alpha protein secretion in breast cancer is associated with poor differentiation and estrogen receptor alpha negativity. Int J Gynecol Cancer 16(Suppl 2):556-559. doi: 10.1111/j.1525-1438.2006.00695.x
102. Bochner BS, Gleich GJ (2010) What targeting eosinophils has taught us about their role in diseases. J Allergy Clin Immunol 126:16-25. doi: 10.1016/j.jaci.2010.02.026 quiz 26-7
103. Molfino NA, Gossage D, Kolbeck R et al (2012) Molecular and clinical rationale for therapeutic targeting of interleukin-5 and its receptor. Clin Exp Allergy 42:712-737. doi: 10.1111/j.1365-2222.2011.03854.x
104. Kolbeck R, Kozhich A, Koike M et al (2010) MEDI-563, a humanized anti-IL-5 receptor alpha mAb with enhanced antibody-dependent cell-mediated cytotoxicity function. J Allergy Clin Immunol 125(1344-1353):e2. doi: 10.1016/j.jaci.2010.04.004
105. Busse WW, Katial R, Gossage D et al (2010) Safety profile, pharmacokinetics, and biologic activity of MEDI-563, an anti-IL-5 receptor alpha antibody, in a phase I study of subjects with mild asthma. J Allergy Clin Immunol 125(1237-1244):e2. doi: 10.1016/j.jaci.2010.04.005
106. Zamarron BF, Chen W (2011) Dual roles of immune cells and their factors in cancer development and progression. Int J Biol Sci 7:651-658
107. Biswas SK, Mantovani A (2010) Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11:889-896. doi: 10.1038/ni.1937