Warning: fopen(/home/virtual/jptm/journal/upload/ip_log/ip_log_2023-02.txt): failed to open stream: Permission denied in /home/virtual/lib/view_data.php on line 83 Warning: fwrite() expects parameter 1 to be resource, boolean given in /home/virtual/lib/view_data.php on line 84 Journal of Pathology and Translational Medicine
Skip Navigation
Skip to contents

JPTM : Journal of Pathology and Translational Medicine

OPEN ACCESS
SEARCH
Search

Articles

Page Path
HOME > J Pathol Transl Med > Volume 49(4); 2015 > Article
Original Article
Cancers with Higher Density of Tumor-Associated Macrophages Were Associated with Poor Survival Rates
Kyong Yeun Jung1,2, Sun Wook Cho1,3, Young A Kim4, Daein Kim3, Byung-Chul Oh5, Do Joon Park1, Young Joo Park,1
Journal of Pathology and Translational Medicine 2015;49(4):318-324.
DOI: https://doi.org/10.4132/jptm.2015.06.01
Published online: June 17, 2015
  • 10,394 Views
  • 196 Download
  • 96 Crossref
  • 113 Scopus

1Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Korea

2Department of Internal Medicine, Eulji University School of Medicine, Seoul, Korea

3Department of Internal Medicine, National Medical Center, Seoul, Korea

4Department of Pathology, SMG-SNU Boramae Medical Center, Seoul, Korea

5Lee Gil Ya Cancer and Diabetes Institute, Gachon University Graduate School of Medicine, Incheon, Korea

Corresponding Author Young Joo Park, MD, PhD Department of Internal Medicine, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 110-799, Korea Tel: +82-2-2072-4183 Fax: +82-2-764-2199 E-mail: yjparkmd@snu.ac.kr
• Received: May 21, 2015   • Accepted: June 1, 2015

© 2015 The Korean Society of Pathologists/The Korean Society for Cytopathology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • Background:
    Macrophages are a component of a tumor’s microenvironment and have various roles in tumor progression and metastasis. This study evaluated the relationships between tumor-associated macrophage (TAM) density and clinical outcomes in 14 different types of human cancers.
  • Methods:
    We investigated TAM density in human tissue microarray sections from 14 different types of human cancers (n = 266) and normal thyroid, lung, and breast tissues (n = 22). The five-year survival rates of each cancer were obtained from the 2011 Korea Central Cancer Registry.
  • Results:
    Among 13 human cancers, excluding thyroid cancer, pancreas, lung, and gallbladder cancers had the highest density of CD163-positive macrophages (7.0±3.5%, 6.9±7.4%, and 6.9 ± 5.5%, respectively). The five-year relative survival rates of these cancers (pancreas, 8.7%; lung, 20.7%; gallbladder, 27.5%) were lower than those of other cancers. The histological subtypes in thyroid cancer exhibited significantly different CD163-positive macrophages densities (papillary, 1.8 ± 1.6% vs anaplastic, 22.9 ± 17.1%; p < .001), but no significant difference between histological subtypes was detected in lung and breast cancers. Moreover, there was no significant difference in CD163-positive macrophages densities among the TNM stages in lung, breast, and thyroid cancers.
  • Conclusions:
    Cancers with higher TAM densities (pancreas, lung, anaplastic thyroid, and gallbladder) were associated with poor survival rate.
The tumor microenvironment includes cancer cells and various stromal cells, including immune cells, fibroblasts, and vascular endothelial cells [1]. Tumor-associated macrophages (TAMs) are also present in the tumor microenvironment and are important in tumor progression and metastasis [2]. TAMs can induce neoplastic cell transformation, elicit tumor destructive reactions, and have either negative or positive effects on tumor growth [3]. Several reports have suggested that TAMs are associated with tumor growth, disease progression, and poor prognosis in some human cancers [4-6]. Moreover, high densities of TAMs are present in the more advanced stages of cancers that have poor prognoses, such as breast [7], lung [8], thyroid [5], and bladder [3] cancers. In contrast, several reports, including those on colorectal [9], stomach [10], lung [11,12], and endometrial [13] cancers, have shown that a high density of TAMs is associated with a high survival rate. Collectively, these results suggest that TAMs can have either positive or negative effects depending on the specific tissue type, tumor location, and tumor stage. The aim of this study was to evaluate the relationship between TAM density and clinical outcome in various human cancers.
Study subjects and tissue microarrays
We purchased 14 different type of human cancer human tissue microarray sections (lung, 49; breast, 49; thyroid, 10; pancreas, 10; gallbladder, 9; larynx, 9; esophagus, 10; liver, 10; cervix, 10; ovary, 10; stomach, 10; prostate, 9; kidney, 9; and endometrium, 9 sections) and normal tissues (lung, 9; breast, 8 sections) from SuperBioChips Laboratories (Seoul, Korea). The supplier provided the clinical information associated with each section, including age at surgery; gender; pathologic diagnosis; TNM staging for cancers; survival/death follow-up result for lung and breast cancers; and estrogen receptor (ER), progesterone receptor (PR), p53, and C-erbB2 expression for breast cancers. Thyroid microarrays contained normal thyroid (n=5), papillary thyroid cancer (PTC; n=35), and anaplastic thyroid cancer (ATC; n=18), and one of the thyroid microarray slides was used in a previous study [14]. Clinical and pathologic data for the thyroid samples were obtained from medical records at Seoul National University Hospital and SMG-SNU Boramae Medical Center. The five-year cancer relative survival rates were obtained from the 2011 annual report of cancer statistics in Korea [15].
Immunohistochemistry on tissue array blocks
CD68 and CD163 were used as TAM markers. Immunohistochemical (IHC) staining for CD68 and CD163 was performed using the BenchMark XT Slide Preparation System (Ventana Medical Systems, Tucson, AZ, USA) and CD68 (ready-to-use, 514H12, Novocastra, Newcastle upon Tyne, UK) and CD163 (1:200, 10D6, ER2, Novocastra). The proportion of CD163-positive area in each tumor was evaluated after IHC staining (Fig. 1). We divided the area of each tissue core into quarters and a central area and randomly chose all five fragments to determine the positive stain proportion (Fig. 1A). Areas of fibrosis or tumor necrosis among the randomly chosen fragments were excluded. We used a color deconvolution plug-in for Image J software to identify the positive stains and to calculate the percent CD163-positive area (Fig. 1B, C). TAM density was determined by calculating the average CD163-positive area (%) at a minimum of four different sites in each tissue.
Statistical analysis
The CD163-positive macrophages density (%) is presented as mean±standard deviation. Differences in CD163-positive macrophages densities among TNM cancer stages, histological subtypes, and pathological characteristics were determined using one-way analysis of variance (ANOVA) or Student’s t test. Statistical significance is indicated by a p-value less than .05. All data were analyzed with IBM SPSS Statistics ver. 20.0 (SPSS Inc., Chicago, IL, USA).
Ethics statement
This study was approved by the Institutional Review Boards of Seoul National University Hospital (1107-060-369) and SMG-SNU Boramae Medical Center (06-2010-176). The need for informed consent was waived by those boards.
CD163-positive macrophage densities and prognoses in human cancers
The average CD163-positive area was significantly correlated with the average CD68-positive area (%) in thyroid (r=0.775, p<.001) (Appendix 1A), breast (r=0.806, p<.001) (Appendix 1B), and lung (r=0.780, p<.001) (Appendix 1C) cancers. Therefore, our remaining IHC assessments were performed with CD163 data.
The CD163-positive macrophages densities and the five-year relative survival rates in the 14 different types of human cancers are summarized in Fig. 2. Excluding thyroid cancer, of the 13 other human cancers, pancreas, lung, and gallbladder cancers had the highest density of CD163-positive macrophages (7.0±3.5%, 6.9±7.4%, and 6.9±5.5%, respectively). In contrast, endometrium, prostate, and kidney cancers had the lowest densities of CD163-positive macrophages (3.6±4.6%, 2.8±2.5%, and 2.8±1.8%, respectively). Interestingly, among the tested cancers, five-year relative survival rate (%) was inversely correlated with CD163-positive macrophages density. The five-year overall survival rates of the cancers with highest TAM densities (pancreas, 8.7%; lung, 20.7%; gallbladder and biliary tract, 27.5%) were lower than those of the cancers with the lowest TAM densities (endometrial, 86.5%; kidney, 78.8%; prostate, 92%).
Of the 14 cancers assessed, thyroid cancer exhibited an extremely wide range of TAM densities that varied according to pathologic subtype (Fig. 3). The ATC cases had the highest density of CD163-positive macrophages (22.9±17.1%), whereas the PTC cases had the lowest CD163-positive macrophage density (1.8±1.3%).
Clinicopathological correlations with TAM density in thyroid, lung, and breast cancers
To investigate the role of TAMs in human cancers, we evaluated the correlations between TAM density and clinicopathological features in lung, breast, and PTC cancers. The CD163-positive macrophage density was significantly higher in cancer tissues than normal tissues in breast (4.7±4.5% vs 0.6±0.2%; p<.001), lung (6.9±7.4% vs 1.6±1.6%; p<.001), and thyroid (PTC, 1.8±1.3% vs normal, 0.2±0.2%; p<.001) tissues (Fig. 3). Among the histological subtypes of lung (adenocarcinoma, 5.8±4.4% vs squamous cell carcinoma, 5.9±4.5% vs large cell carcinoma, 8.7±7.3%; p=.428) and breast cancers (infiltrating ductal carcinoma, 4.0±3.4% vs medullary carcinoma, 9.3±3.4%; p=.055), there were no significant differences in CD163-positive macrophages density (Appendix 2). Differences among TNM stages were evaluated by assessing adenocarcinoma and squamous cell carcinoma of lung cancer, infiltrating ductal carcinoma of breast cancer, and PTC. There were no significant differences in CD163-positive macrophage density associated with TNM stage in lung (p=.821), breast (p=.060), or thyroid (PTC, p=.943) cancer (Appendix 2). Within the breast cancer samples, several prognostic markers including ER, PR, p53, and C-erbB2 were analyzed. The ER-positive (3.4±4.5% vs 5.6±4.8%; p=.182) and PR-positive (3.7±4.4% vs 5.4±4.9%; p=.319) breast cancers showed non-significant trends toward lower CD163-positive macrophages density than those in the ER- or PR-negative breast cancers. In contrast, p53-positive (5.9±5.9% vs 4.2±3.6%; p=.269) and C-erbB2-positive (6.4±6.8% vs 4.4±3.8%; p=.233) breast cancer showed nonsignificant trends toward higher CD163-positive macrophage density than those in p53- or C-erbB2-negative breast cancers.
Our results demonstrate that CD163-positive macrophage density is inversely correlated with five-year cancer survival rate in a variety of human cancers. This finding suggests the presence of a potential pro-tumorigenic role of TAMs in some human cancers. Among the 14 different types of human cancers assessed, ATC, the most aggressive cancer in humans [16,17], had the highest CD163-positive macrophages density (23%), which was markedly higher than the second highest TAM density (7%) detected in the pancreas cancer samples. ATC accounts for up to 2% of thyroid cancers and is characterized by an extremely poor survival rate with a one-year average survival rate of 20% and a median survival duration of five months [18,19]. In contrast, the most common well-differentiated thyroid cancer, PTC, had the lowest CD163-positive macrophages density (1.8%). PTC is associated with lower recurrence and mortality rates [20] than other solid and relatively indolent tumors and has a five-year survival rate higher than 90% [15]. Since the differentiation of pathologic subtypes is distinctive and survival rates markedly differ among subtypes, our observation of a striking difference in CD163-positive macrophages density between two thyroid cancer subtypes led us to hypothesize that TAM density is a potential prognostic factor in human cancers.
In contrast, histological subtypes of lung and breast cancers did not exhibit significant differences in CD163-positive macrophage density. Correlations between TAM density and clinicopathological features have been reported in ductal and lobular carcinomas in breast cancer [21,22] and in adenocarcinoma [23,24] and non-small cell [25,26] lung cancers. Nonetheless, only a few reports have compared TAM density based on histological subtype. Although our data did not detect a significant difference related to histological subtype in lung or breast cancers, the number of each subtype in our sample population was limited. Therefore, we recommend a larger-scale study of TAM density in a variety of histological subtypes.
In this study, there were no significant differences in CD163-positive macrophage density among TNM stages in lung, breast, or thyroid cancers. In addition, cancer tissues showed higher CD163-positive macrophage densities than those in normal tissues in lung, breast, and thyroid samples. In breast cancer, there were trends toward negative correlations of TAM density with ER and PR expression, whereas there were trends toward positive correlations of TAM density with p53 and C-erbB2 expression. Previous reports indicate that TAM infiltration is inversely correlated with ER expression in breast cancer [7,27]. However, this correlation might vary with TAM location [22]. Medrek et al. [22] reported that a dense infiltration of CD163-positive macrophages in tumor stroma was associated with ER- and PR-negativity, but there was no such association in tumor nest. Our study results show a non-significant trend toward negative correlations between ER and PR expressions and density of CD163-positive macrophages. Due to data limitations, we could not assess such correlations according to infiltration location.
Selecting the most appropriate marker for TAM assessment can be challenging. Originally, a TAM was seen as a residual macrophage within the tumor microenvironment, and the biological characteristics of TAMs have been shown to be anti-tumorigenic, cytotoxic, or pro-tumorigenic [1,28]. Furthermore, macrophages can undergo polarization and change from an M1-macrophage (classically activated, pro-inflammatory) to an M2-macrophage (alternatively activated, anti-inflammatory or regenerative) [29]. Collectively, these findings indicate the difficulty in choosing a cancer-specific TAM marker. In the beginning of this study, we performed IHC investigations using both CD68, a pan macrophage marker [29], and CD163, a more specific marker for M2-macrophages [30]. Those investigations revealed that the CD163-positive areas were significantly positively correlated with the CD68-positive areas in lung, breast, and thyroid cancers; thus, our remaining IHC assessments were performed with CD163 data.
Previous clinical studies have shown a correlation between TAM density and cancer prognosis. Most studies have shown a significant correlation between TAM density and poor prognosis, especially among breast, thyroid, and lung cancers [5,7,8,22]. However, several studies have reported that TAM density is associated with good prognosis. Such contradictory results might be due to differences in the number, grade, stage, or size of tumors among the studies. In addition, previous clinical studies have used various methods to assess TAM infiltration. The use of different approaches could have also contributed to the inconsistent results. Although the sample size for each cancer subtype in our study population was small, the results in this study comparing TAM density in various human cancers are significant; therefore, further studies with larger sample sizes are warranted.
In summary, we detected a trend toward an inverse correlation between CD163-positive macrophage density and five-year survival rate in 14 different types of human cancers. In particular, PTC and ATC clearly showed an inverse correlation between TAM density and prognosis. Our results suggest that TAM density is a potential biomarker of poor prognosis in human cancers.

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

This work was supported by a grant from the Next-Generation BioGreen 21 Program (No.PJ00954003), Rural Development Administration, Republic of Korea.
Fig. 1.
Immunohistochemical staining for CD163 in breast cancer. Representative CD163 staining in breast cancer. TAM density was measured by averaging the CD163-positive area (%) of five different sites in each tissue (A). The positive IHC staining area (%) was separated and calculated using the Image J color deconvolution plugin (B, C).
jptm-49-4-318f1.gif
Fig. 2.
CD163-positive macrophage densities and five-year survival rates in 14 different types of human cancers. Left axis and bar graphs represent the average CD163-positive area (%) as mean ± standard error. Right axis and star-shaped markers represent the five-year overall survival (OS, %) obtained from the 2011 Annual Report of Cancer Statistics in Korea. PTC, papillary thyroid cancer; GB, gallbladder; ATC, anaplastic thyroid cancer; NA, not acquired.
jptm-49-4-318f2.gif
Fig. 3.
The CD163-positive macrophage densities of normal tissue, papillary thyroid cancer (PTC) and anaplastic thyroid cancer (ATC).
jptm-49-4-318f3.gif
  • 1. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420: 860–7. ArticlePubMedPMC
  • 2. Cho SW. Interactions between immune cells and tumor cells. J Korean Thyroid Assoc 2013; 6: 96–100. Article
  • 3. Zhang QW, Liu L, Gong CY, et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One 2012; 7: e50946. Article
  • 4. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002; 196: 254–65. ArticlePubMed
  • 5. Kim S, Cho SW, Min HS, et al. The expression of tumor-associated macrophages in papillary thyroid carcinoma. Endocrinol Metab (Seoul) 2013; 28: 192–8. ArticlePubMedPMC
  • 6. Zeni E, Mazzetti L, Miotto D, et al. Macrophage expression of interleukin-10 is a prognostic factor in nonsmall cell lung cancer. Eur Respir J 2007; 30: 627–32. ArticlePubMed
  • 7. Campbell MJ, Tonlaar NY, Garwood ER, et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res Treat 2011; 128: 703–11. ArticlePubMed
  • 8. Sato S, Hanibuchi M, Kuramoto T, et al. Macrophage stimulating protein promotes liver metastases of small cell lung cancer cells by affecting the organ microenvironment. Clin Exp Metastasis 2013; 30: 333–44. ArticlePubMed
  • 9. Forssell J, Oberg A, Henriksson ML, Stenling R, Jung A, Palmqvist R. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin Cancer Res 2007; 13: 1472–9. ArticlePubMed
  • 10. Ohno S, Inagawa H, Dhar DK, et al. The degree of macrophage infiltration into the cancer cell nest is a significant predictor of survival in gastric cancer patients. Anticancer Res 2003; 23: 5015–22. PubMed
  • 11. Welsh TJ, Green RH, Richardson D, Waller DA, O’Byrne KJ, Bradding P. Macrophage and mast-cell invasion of tumor cell islets confers a marked survival advantage in non-small-cell lung cancer. J Clin Oncol 2005; 23: 8959–67. ArticlePubMed
  • 12. Kawai O, Ishii G, Kubota K, et al. Predominant infiltration of macrophages and CD8(+) T cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer 2008; 113: 1387–95. ArticlePubMed
  • 13. Ohno S, Ohno Y, Suzuki N, et al. Correlation of histological localization of tumor-associated macrophages with clinicopathological features in endometrial cancer. Anticancer Res 2004; 24: 3335–42. PubMed
  • 14. Cho SW, Kim YA, Sun HJ, et al. Therapeutic potential of Dickkopf-1 in wild-type BRAF papillary thyroid cancer via regulation of betacatenin/E-cadherin signaling. J Clin Endocrinol Metab 2014; 99: E1641–9. PubMed
  • 15. Jung KW, Won YJ, Kong HJ, Oh CM, Lee DH, Lee JS. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2011. Cancer Res Treat 2014; 46: 109–23. ArticlePubMedPMCPDF
  • 16. Cornett WR, Sharma AK, Day TA, et al. Anaplastic thyroid carcinoma: an overview. Curr Oncol Rep 2007; 9: 152–8. ArticlePubMed
  • 17. Are C, Shaha AR. Anaplastic thyroid carcinoma: biology, pathogenesis, prognostic factors, and treatment approaches. Ann Surg Oncol 2006; 13: 453–64. ArticlePubMed
  • 18. Smallridge RC, Copland JA. Anaplastic thyroid carcinoma: pathogenesis and emerging therapies. Clin Oncol (R Coll Radiol) 2010; 22: 486–97. ArticlePubMedPMC
  • 19. Haymart MR, Banerjee M, Yin H, Worden F, Griggs JJ. Marginal treatment benefit in anaplastic thyroid cancer. Cancer 2013; 119: 3133–9. ArticlePubMedPMC
  • 20. Lin JD, Chen ST, Hsueh C, Chao TC. A 29-year retrospective review of papillary thyroid cancer in one institution. Thyroid 2007; 17: 535–41. ArticlePubMed
  • 21. Murri AM, Hilmy M, Bell J, et al. The relationship between the systemic inflammatory response, tumour proliferative activity, T-lymphocytic and macrophage infiltration, microvessel density and survival in patients with primary operable breast cancer. Br J Cancer 2008; 99: 1013–9. ArticlePubMedPMC
  • 22. Medrek C, Pontén F, Jirström K, Leandersson K. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer 2012; 12: 306.ArticlePubMedPMC
  • 23. Ohtaki Y, Ishii G, Nagai K, et al. Stromal macrophage expressing CD204 is associated with tumor aggressiveness in lung adenocarcinoma. J Thorac Oncol 2010; 5: 1507–15. ArticlePubMed
  • 24. Zhang BC, Gao J, Wang J, Rao ZG, Wang BC, Gao JF. Tumor-associated macrophages infiltration is associated with peritumoral lymphangiogenesis and poor prognosis in lung adenocarcinoma. Med Oncol 2011; 28: 1447–52. ArticlePubMed
  • 25. Ma J, Liu L, Che G, Yu N, Dai F, You Z. The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer 2010; 10: 112.ArticlePubMedPMC
  • 26. Al-Shibli K, Al-Saad S, Donnem T, Persson M, Bremnes RM, Busund LT. The prognostic value of intraepithelial and stromal innate immune system cells in non-small cell lung carcinoma. Histopathology 2009; 55: 301–12. ArticlePubMed
  • 27. Steele RJ, Eremin O, Brown M, Hawkins RA. Oestrogen receptor concentration and macrophage infiltration in human breast cancer. Eur J Surg Oncol 1986; 12: 273–6. PubMed
  • 28. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004; 4: 71–8. ArticlePubMed
  • 29. Heusinkveld M, van der Burg SH. Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med 2011; 9: 216.ArticlePubMedPMC
  • 30. Ambarus CA, Krausz S, van Eijk M, et al. Systematic validation of specific phenotypic markers for in vitro polarized human macrophages. J Immunol Methods 2012; 375: 196–206. ArticlePubMed
Appendix 1.
The correlation between average CD163-positive area (%) and average CD68-positivie area (%). (A) Thyroid cancer. (B) Breast cancer. (C) Lung cancer.
jptm-49-4-318a1.gif
Appendix 2.
Average CD163-positive area (%) according to clinicopathologic characteristics in lung, breast, and thyroid cancer
Charaacteristic No. CD163 (%) p-valuea
Lung
 Histology
  Adenocarcinoma 19 5.8 ± 4.4 .428
  SQCC 20 5.9 ± 4.5
  Large cell carcinoma 4 8.7 ± 7.3
  SCC 2 1.0 ± 0.5
  Mixed carcinoma 4 5.0 ± 2.3
 Stageb
  I 16 5.7 ± 4.4 .821
  II 12 6.6 ± 5.2
  III 10 5.5 ± 3.8
  IV 1 2.4
 Survival
  Alive 15 3.6 ± 3.4 .104
  Death 15 5.9 ± 3.9
Breast
 Infiltrating ductal 45 4.0 ± 3.4 .055
 Medullary 2 9.3 ± 3.4
 Sarcomatoid 1 1.9
 Metaplastic 1 10.1
 Stageb
  IIA 13 5.3 ± 4.9 .060
  IIB 10 4.2 ± 2.4
  IIIA 12 1.8 ± 1.4
  IIIB 10 4.5 ± 2.3
 Alive 30 4.2 ± 3.7 .726
 Death 6 3.7 ± 2.5
Thyroid
 PTC 35 1.8 ± 1.3 < .001
 ATC 18 22.9 ± 17.1
 Stageb
  I 3 1.4 ± 0.6 .943
  II 3 1.7 ± 1.1
  III 21 1.8 ± 1.2
  IV 4 1.8 ± 0.8
 Alive 15 1.8 ± 1.5 .241
 Death 2 3.3 ± 2.8

SQCC, squamous cell carcinoma; SCC; small cell carcinoma, PTC; papillary thyroid carcinoma, ATC; anaplastic thyroid carcinoma.

a p-value by ANOVA or student t test;

b TNM stage and survival was classified in adenocarcinoma and squamous cell carcinoma (lung), infiltrating ductal carcinoma (breast) and papillary thyroid carcinoma (thyroid).

Figure & Data

References

    Citations

    Citations to this article as recorded by  
    • Are third-generation active-targeting nanoformulations definitely the best? In vitro and in vivo comparisons of pixantrone-loaded liposomes modified with different sialic acid derivatives
      Yanzhi Song, Zhennan She, Zhenjun Huang, Shuo Wang, Xinrong Liu, Qi Zhang, Jing Sun, Donghua Di, Yihui Deng
      Drug Delivery and Translational Research.2022; 12(3): 647.     CrossRef
    • Synergistic nanoassemblies constructed from a STAT3 inhibitor and a cabazitaxel prodrug with enhanced cancer chemo-immunotherapy
      X. Shi, L. Shu, Y. Qiao, J. Yao, H. Xie, L. Zhou, H. Wang, S. Zheng
      Materials Today Nano.2022; 17: 100155.     CrossRef
    • Polypharmacologic Reprogramming of Tumor-Associated Macrophages toward an Inflammatory Phenotype
      Nao Nishida-Aoki, Taranjit S. Gujral
      Cancer Research.2022; 82(3): 433.     CrossRef
    • Role of Suprabasin in the Dedifferentiation of Follicular Epithelial Cell-Derived Thyroid Cancer and Identification of Related Immune Markers
      Hao Tan, Lidong Wang, Zhen Liu
      Frontiers in Genetics.2022;[Epub]     CrossRef
    • Macrophage C/EBPδ Drives Gemcitabine, but Not 5-FU or Paclitaxel, Resistance of Pancreatic Cancer Cells in a Deoxycytidine-Dependent Manner
      C. Arnold Spek, Hella L. Aberson, JanWillem Duitman
      Biomedicines.2022; 10(2): 219.     CrossRef
    • Anaplastic Thyroid Carcinoma: An Update
      Arnaud Jannin, Alexandre Escande, Abir Al Ghuzlan, Pierre Blanchard, Dana Hartl, Benjamin Chevalier, Frédéric Deschamps, Livia Lamartina, Ludovic Lacroix, Corinne Dupuy, Eric Baudin, Christine Do Cao, Julien Hadoux
      Cancers.2022; 14(4): 1061.     CrossRef
    • LC3-associated phagocytosis in bone marrow macrophages suppresses acute myeloid leukemia progression through STING activation
      Jamie A. Moore, Jayna J. Mistry, Charlotte Hellmich, Rebecca H. Horton, Edyta E. Wojtowicz, Aisha Jibril, Matthew Jefferson, Thomas Wileman, Naiara Beraza, Kristian M. Bowles, Stuart A. Rushworth
      Journal of Clinical Investigation.2022;[Epub]     CrossRef
    • Integration of chemokine signaling with non-coding RNAs in tumor microenvironment and heterogeneity in different cancers
      Shweta Arora, Salman Khan, Almaz Zaki, Gulnaz Tabassum, Mohd Mohsin, Humaira Naaz Bhutto, Tanveer Ahmad, Tasneem Fatma, Mansoor Ali Syed
      Seminars in Cancer Biology.2022; 86: 720.     CrossRef
    • BRAFV600E Induction in Thyrocytes Triggers Important Changes in the miRNAs Content and the Populations of Extracellular Vesicles Released in Thyroid Tumor Microenvironment
      Ophélie Delcorte, Catherine Spourquet, Pascale Lemoine, Jonathan Degosserie, Patrick Van Der Smissen, Nicolas Dauguet, Axelle Loriot, Jeffrey A. Knauf, Laurent Gatto, Etienne Marbaix, James A. Fagin, Christophe E. Pierreux
      Biomedicines.2022; 10(4): 755.     CrossRef
    • Inflammatory Tumor Microenvironment in Cranial Meningiomas: Clinical Implications and Intraindividual Reproducibility
      Johannes Wach, Tim Lampmann, Ági Güresir, Hartmut Vatter, Ulrich Herrlinger, Albert Becker, Marieta Toma, Michael Hölzel, Erdem Güresir
      Diagnostics.2022; 12(4): 853.     CrossRef
    • Roles and new Insights of Macrophages in the Tumor Microenvironment of Thyroid Cancer
      Qi Liu, Wei Sun, Hao Zhang
      Frontiers in Pharmacology.2022;[Epub]     CrossRef
    • Fucoxanthin Is a Potential Therapeutic Agent for the Treatment of Breast Cancer
      Tsz-Ying Lau, Hiu-Yee Kwan
      Marine Drugs.2022; 20(6): 370.     CrossRef
    • Dissecting Immunosuppressive Cell Communication Patterns Reveals JunB Proto-Oncogene (JUNB) Shaping a Non-Inflamed Tumor Microenvironment
      Hualin Chen, Gang Chen
      Frontiers in Genetics.2022;[Epub]     CrossRef
    • LIMK1: A promising prognostic and immune infiltration indicator in colorectal cancer
      Xin Liu, Qiang Song, Daohan Wang, Yubiao Liu, Zhixiang Zhang, Weihua Fu
      Oncology Letters.2022;[Epub]     CrossRef
    • Unusual Association of NF-κB Components in Tumor-Associated Macrophages (TAMs) Promotes HSPG2-Mediated Immune-Escaping Mechanism in Breast Cancer
      Veronica De Paolis, Fabio Maiullari, Maila Chirivì, Marika Milan, Chiara Cordiglieri, Francesca Pagano, Alessandra Rita La Manna, Elena De Falco, Claudia Bearzi, Roberto Rizzi, Chiara Parisi
      International Journal of Molecular Sciences.2022; 23(14): 7902.     CrossRef
    • Crosstalk between angiogenesis and immune regulation in the tumor microenvironment
      Hei Jung Kim, Young Rae Ji, You Mie Lee
      Archives of Pharmacal Research.2022; 45(6): 401.     CrossRef
    • Cancer Resistance to Immunotherapy: Molecular Mechanisms and Tackling Strategies
      Son Hai Vu, Preethi Vetrivel, Jongmin Kim, Myeong-Sok Lee
      International Journal of Molecular Sciences.2022; 23(18): 10906.     CrossRef
    • Transcription Factor MAFB as a Prognostic Biomarker for the Lung Adenocarcinoma
      Omar Samir, Naohiro Kobayashi, Teppei Nishino, Mennatullah Siyam, Manoj Kumar Yadav, Yuri Inoue, Satoru Takahashi, Michito Hamada
      International Journal of Molecular Sciences.2022; 23(17): 9945.     CrossRef
    • Construction and Validation of a CNV-Driven Ferroptosis-Related Gene Signature for Predicting the Prognosis of Lung Adenocarcinoma
      Yanqing Wang, Yi Zhao, Yong Li, Zemin Luo, Hongzhu Chen, Yuan Li
      Journal of Sensors.2022; 2022: 1.     CrossRef
    • CXCL12 derived from CD248-expressing cancer-associated fibroblasts mediates M2-polarized macrophages to promote nonsmall cell lung cancer progression
      Jieheng Wu, Xinlei Liu, Jiangwei Wu, Chunju Lou, Qiaoling Zhang, Huiping Chen, Zeyang Yang, Shiqi Long, Yun Wang, Zhenling Shang, Zuquan Hu, Rui Zhang, Jian Zhang, Zhu Zeng
      Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease.2022; 1868(11): 166521.     CrossRef
    • Cell Component and Function of Tumor Microenvironment in Thyroid Cancer
      Eunah Shin, Ja Seung Koo
      International Journal of Molecular Sciences.2022; 23(20): 12578.     CrossRef
    • TIM3 Expression in Anaplastic-Thyroid-Cancer-Infiltrating Macrophages: An Emerging Immunotherapeutic Target
      Luz Maria Palacios, Victoria Peyret, María Estefania Viano, Romina Celeste Geysels, Yair Aron Chocobar, Ximena Volpini, Claudia Gabriela Pellizas, Juan Pablo Nicola, Claudia Cristina Motran, María Cecilia Rodriguez-Galan, Laura Fozzatti
      Biology.2022; 11(11): 1609.     CrossRef
    • Potential diagnostic of lymph node metastasis and prognostic values of TM4SFs in papillary thyroid carcinoma patients
      Kun Wang, Haomin Li, Junyu Zhao, Jinming Yao, Yiran Lu, Jianjun Dong, Jie Bai, Lin Liao
      Frontiers in Cell and Developmental Biology.2022;[Epub]     CrossRef
    • A distinct M2 macrophage infiltrate and transcriptomic profile decisively influence adipocyte differentiation in lipedema
      Stefan Wolf, Jenna H. Rannikko, Reetta Virtakoivu, Paolo Cinelli, Gunther Felmerer, Anna Burger, Pietro Giovanoli, Michael Detmar, Nicole Lindenblatt, Maija Hollmén, Epameinondas Gousopoulos
      Frontiers in Immunology.2022;[Epub]     CrossRef
    • Macrophage targeting in cancer
      Martha Lopez‐Yrigoyen, Luca Cassetta, Jeffrey W. Pollard
      Annals of the New York Academy of Sciences.2021; 1499(1): 18.     CrossRef
    • Immune Landscape of Thyroid Cancers: New Insights
      Elisa Menicali, Martina Guzzetti, Silvia Morelli, Sonia Moretti, Efisio Puxeddu
      Frontiers in Endocrinology.2021;[Epub]     CrossRef
    • Targeting tumor-associated macrophages to synergize tumor immunotherapy
      Xiaonan Xiang, Jianguo Wang, Di Lu, Xiao Xu
      Signal Transduction and Targeted Therapy.2021;[Epub]     CrossRef
    • FOXE1-Dependent Regulation of Macrophage Chemotaxis by Thyroid Cells In Vitro and In Vivo
      Sara Credendino, Marta De Menna, Irene Cantone, Carmen Moccia, Matteo Esposito, Luigi Di Guida, Mario De Felice, Gabriella De Vita
      International Journal of Molecular Sciences.2021; 22(14): 7666.     CrossRef
    • Hidden Treasures: Macrophage Long Non-Coding RNAs in Lung Cancer Progression
      Annika Karger, Rajender Nandigama, Albrecht Stenzinger, Friedrich Grimminger, Soni Savai Pullamsetti, Werner Seeger, Rajkumar Savai
      Cancers.2021; 13(16): 4127.     CrossRef
    • A Prognostic Role for Circulating microRNAs Involved in Macrophage Polarization in Advanced Non-Small Cell Lung Cancer
      Alexia Monastirioti, Chara Papadaki, Konstantinos Rounis, Despoina Kalapanida, Dimitrios Mavroudis, Sofia Agelaki
      Cells.2021; 10(8): 1988.     CrossRef
    • Hyperglycemia-Induced miR-467 Drives Tumor Inflammation and Growth in Breast Cancer
      Jasmine Gajeton, Irene Krukovets, Santoshi Muppala, Dmitriy Verbovetskiy, Jessica Zhang, Olga Stenina-Adognravi
      Cancers.2021; 13(6): 1346.     CrossRef
    • Targeting MARCO and IL37R on Immunosuppressive Macrophages in Lung Cancer Blocks Regulatory T Cells and Supports Cytotoxic Lymphocyte Function
      Linnéa La Fleur, Johan Botling, Fei He, Catarina Pelicano, Chikai Zhou, Chenfei He, Giorgia Palano, Artur Mezheyeuski, Patrick Micke, Jeffrey V. Ravetch, Mikael C. I. Karlsson, Dhifaf Sarhan
      Cancer Research.2021; 81(4): 956.     CrossRef
    • Absent in melanoma 2-mediating M1 macrophages facilitate tumor rejection in renal carcinoma
      Dafei Chai, Zichun Zhang, Shang yuchen Shi, Dong Qiu, Chen Zhang, Gang Wang, Lin Fang, Huizhong Li, Hui Tian, Hailong Li, Junnian Zheng
      Translational Oncology.2021; 14(4): 101018.     CrossRef
    • Hampering Stromal Cells in the Tumor Microenvironment as a Therapeutic Strategy to Destem Cancer Stem Cells
      Katherine Po Sin Chung, Rainbow Wing Hei Leung, Terence Kin Wah Lee
      Cancers.2021; 13(13): 3191.     CrossRef
    • Thyroid Cancer Stem-Like Cells: From Microenvironmental Niches to Therapeutic Strategies
      Elisa Stellaria Grassi, Viola Ghiandai, Luca Persani
      Journal of Clinical Medicine.2021; 10(7): 1455.     CrossRef
    • Enhanced Drug Delivery to Solid Tumors via Drug-Loaded Nanocarriers: An Image-Based Computational Framework
      Farshad Moradi Kashkooli, M. Soltani, Mohammad Masoud Momeni, Arman Rahmim
      Frontiers in Oncology.2021;[Epub]     CrossRef
    • Mechanisms of primary and acquired resistance to PD-1/PD-L1 blockade and the emerging role of gut microbiome
      R. Zou, Y. Wang, F. Ye, X. Zhang, M. Wang, S. Cui
      Clinical and Translational Oncology.2021; 23(11): 2237.     CrossRef
    • Role of Tumor-Associated Macrophages in Sarcomas
      Tomohiro Fujiwara, John Healey, Koichi Ogura, Aki Yoshida, Hiroya Kondo, Toshiaki Hata, Miho Kure, Hiroshi Tazawa, Eiji Nakata, Toshiyuki Kunisada, Toshiyoshi Fujiwara, Toshifumi Ozaki
      Cancers.2021; 13(5): 1086.     CrossRef
    • Secreted Factors by Anaplastic Thyroid Cancer Cells Induce Tumor-Promoting M2-like Macrophage Polarization through a TIM3-Dependent Mechanism
      Cinthia Carolina Stempin, Romina Celeste Geysels, Sunmi Park, Luz Maria Palacios, Ximena Volpini, Claudia Cristina Motran, Eva Virginia Acosta Rodríguez, Juan Pablo Nicola, Sheue-yann Cheng, Claudia Gabriela Pellizas, Laura Fozzatti
      Cancers.2021; 13(19): 4821.     CrossRef
    • Papillary Thyroid Carcinoma Landscape and Its Immunological Link With Hashimoto Thyroiditis at Single-Cell Resolution
      Jun Pan, Fang Ye, Chengxuan Yu, Qinsheng Zhu, Jiaqi Li, Yaohui Zhang, Hedi Tian, Yunjin Yao, Minjie Zhu, Yibin Shen, Feng Zhu, Yingying Wang, Xinhui Zhou, Guoji Guo, Yijun Wu
      Frontiers in Cell and Developmental Biology.2021;[Epub]     CrossRef
    • Evaluation of solid tumor response to sequential treatment cycles via a new computational hybrid approach
      Farshad Moradi Kashkooli, M. Soltani
      Scientific Reports.2021;[Epub]     CrossRef
    • Assessment of outcomes and novel immune biomarkers in metaplastic breast cancer: a single institution retrospective study
      Evan Morgan, Anupama Suresh, Akaansha Ganju, Daniel G. Stover, Robert Wesolowski, Sagar Sardesai, Anne Noonan, Raquel Reinbolt, Jeffrey VanDeusen, Nicole Williams, Mathew A. Cherian, Zaibo Li, Gregory Young, Marilly Palettas, Julie Stephens, Joseph Liu, A
      World Journal of Surgical Oncology.2020;[Epub]     CrossRef
    • Differentiated agonistic antibody targeting CD137 eradicates large tumors without hepatotoxicity
      Ugur Eskiocak, Wilson Guzman, Benjamin Wolf, Christine Cummings, Lauren Milling, Hsin-Jung Wu, Michael Ophir, Conner Lambden, Pearl Bakhru, Dana C. Gilmore, Samantha Ottinger, Lucy Liu, William K. McConaughy, Sunny Q. He, Chao Wang, Cheuk Lun Leung, Jason
      JCI Insight.2020;[Epub]     CrossRef
    • The Tumor Microenvironment: A Milieu Hindering and Obstructing Antitumor Immune Responses
      Alireza Labani-Motlagh, Mehrnoush Ashja-Mahdavi, Angelica Loskog
      Frontiers in Immunology.2020;[Epub]     CrossRef
    • Sevoflurane depletes macrophages from the melanoma microenvironment
      Isabella Sztwiertnia, Judith Schenz, Katharina Bomans, Dominik Schaack, Johanna Ohnesorge, Sandra Tamulyte, Markus A. Weigand, Florian Uhle, Roger Chammas
      PLOS ONE.2020; 15(5): e0233789.     CrossRef
    • Lung cancer aggressiveness in an intermittent hypoxia murine model of postmenopausal sleep apnea
      Marta Torres, Miguel Ángel Martinez-Garcia, Francisco Campos-Rodriguez, David Gozal, Josep M. Montserrat, Daniel Navajas, Ramon Farré, Isaac Almendros
      Menopause.2020; 27(6): 706.     CrossRef
    • Neck Disability and Swallowing Function in Posttreatment Head and Neck Cancer Patients
      Alexandria Harris, Lingyun Lyu, Tamara Wasserman-Winko, Susan George, Jonas T. Johnson, Marci Lee Nilsen
      Otolaryngology–Head and Neck Surgery.2020; 163(4): 763.     CrossRef
    • Metabolic modulation via mTOR pathway and anti-angiogenesis remodels tumor microenvironment using PD-L1-targeting codelivery
      Binfan Chen, Ang Gao, Bin Tu, Yonghui Wang, Xiaolu Yu, Yingshu Wang, Yanfeng Xiu, Bing Wang, Yakun Wan, Yongzhuo Huang
      Biomaterials.2020; 255: 120187.     CrossRef
    • The Thyroid Tumor Microenvironment: Potential Targets for Therapeutic Intervention and Prognostication
      Laura MacDonald, Jonathan Jenkins, Grace Purvis, Joshua Lee, Aime T. Franco
      Hormones and Cancer.2020; 11(5-6): 205.     CrossRef
    • The Contribution of Race to Breast Tumor Microenvironment Composition and Disease Progression
      Gina Kim, Jessica M. Pastoriza, John S. Condeelis, Joseph A. Sparano, Panagiota S. Filippou, George S. Karagiannis, Maja H. Oktay
      Frontiers in Oncology.2020;[Epub]     CrossRef
    • Prognosis of Macrophage Density in the Absence of Neutrophils in Differentiated Thyroid Cancer
      Amblessed E. Onuma, Lynn Schoenfield, Chengli Shen, Charity Edwards, John E. Phay, Lawrence A. Shirley, Allan Tsung
      Journal of Surgical Research.2020; 256: 458.     CrossRef
    • Targeting of CD163+ Macrophages in Inflammatory and Malignant Diseases
      Maria K. Skytthe, Jonas Heilskov Graversen, Søren K. Moestrup
      International Journal of Molecular Sciences.2020; 21(15): 5497.     CrossRef
    • Synthetic chlorin derivative self-prevented from aggregation: Behavior in homogeneous medium for PDT applications
      Bianca Martins Estevão, Camila Fabiano de Freitas, Douglas Santana Franciscato, Francisco Fávaro de Assis, Kleber Thiago de Oliveira, Noboru Hioka, Wilker Caetano, Edvani Curti Muniz
      Journal of Molecular Liquids.2020; 320: 114363.     CrossRef
    • Tumor‑associated macrophages in lung cancer: Friendly or evil? (Review)
      Fei Xu, Ying Wei, Zhao Tang, Baojun Liu, Jingcheng Dong
      Molecular Medicine Reports.2020;[Epub]     CrossRef
    • Macrophage-secreted MMP9 induces mesenchymal transition in pancreatic cancer cells via PAR1 activation
      Cansu Tekin, Hella L Aberson, Cynthia Waasdorp, Gerrit K J Hooijer, Onno J de Boer, Frederike Dijk, Maarten F Bijlsma, C Arnold Spek
      Cellular Oncology.2020; 43(6): 1161.     CrossRef
    • Cancer Stem Cells in Thyroid Tumors: From the Origin to Metastasis
      Veronica Veschi, Francesco Verona, Melania Lo Iacono, Caterina D'Accardo, Gaetana Porcelli, Alice Turdo, Miriam Gaggianesi, Stefano Forte, Dario Giuffrida, Lorenzo Memeo, Matilde Todaro
      Frontiers in Endocrinology.2020;[Epub]     CrossRef
    • The Crosstalk Between Tumor-Associated Macrophages (TAMs) and Tumor Cells and the Corresponding Targeted Therapy
      Zhe Ge, Shuzhe Ding
      Frontiers in Oncology.2020;[Epub]     CrossRef
    • Immune Cell Confrontation in the Papillary Thyroid Carcinoma Microenvironment
      Zhenyu Xie, Xin Li, Yuzhen He, Song Wu, Shiyue Wang, Jianjian Sun, Yuchen He, Yu Lun, Jian Zhang
      Frontiers in Endocrinology.2020;[Epub]     CrossRef
    • Early macrophage infiltrates impair pancreatic cancer cell growth by TNF-α secretion
      Cansu Tekin, Hella L. Aberson, Maarten F. Bijlsma, C. Arnold Spek
      BMC Cancer.2020;[Epub]     CrossRef
    • Attenuation of CD47-SIRPα Signal in Cholangiocarcinoma Potentiates Tumor-Associated Macrophage-Mediated Phagocytosis and Suppresses Intrahepatic Metastasis
      Kulthida Vaeteewoottacharn, Ryusho Kariya, Phattarin Pothipan, Sawako Fujikawa, Chawalit Pairojkul, Sakda Waraasawapati, Kazuhiko Kuwahara, Chaisiri Wongkham, Sopit Wongkham, Seiji Okada
      Translational Oncology.2019; 12(2): 217.     CrossRef
    • Circulating CEA-dNLR score predicts clinical outcome of metastatic gallbladder cancer patient
      Jing-Hui Du, Jun Lu
      Journal of Clinical Laboratory Analysis.2019; 33(2): e22684.     CrossRef
    • The Interplay between MicroRNAs and Cellular Components of Tumour Microenvironment (TME) on Non-Small-Cell Lung Cancer (NSCLC) Progression
      Sook Shien Lee, Yoke Kqueen Cheah
      Journal of Immunology Research.2019; 2019: 1.     CrossRef
    • Papillary thyroid carcinoma behavior: clues in the tumor microenvironment
      Kensey Bergdorf, Donna C Ferguson, Mitra Mehrad, Kim Ely, Thomas Stricker, Vivian L Weiss
      Endocrine-Related Cancer.2019; 26(6): 601.     CrossRef
    • Interplay between thyroid cancer cells and macrophages: effects on IL-32 mediated cell death and thyroid cancer cell migration
      Yvette J. E. Sloot, Katrin Rabold, Thomas Ulas, Dennis M. De Graaf, Bas Heinhuis, Kristian Händler, Joachim L. Schultze, Mihai G. Netea, Johannes W. A. Smit, Leo A. B. Joosten, Romana T. Netea-Maier
      Cellular Oncology.2019; 42(5): 691.     CrossRef
    • Iron accumulation in tumor-associated macrophages marks an improved overall survival in patients with lung adenocarcinoma
      Carl Maximilian Thielmann, Milene Costa da Silva, Thomas Muley, Michael Meister, Esther Herpel, Martina U. Muckenthaler
      Scientific Reports.2019;[Epub]     CrossRef
    • The Immune Landscape of Thyroid Cancer in the Context of Immune Checkpoint Inhibition
      Gilda Varricchi, Stefania Loffredo, Giancarlo Marone, Luca Modestino, Poupak Fallahi, Silvia Martina Ferrari, Amato de Paulis, Alessandro Antonelli, Maria Rosaria Galdiero
      International Journal of Molecular Sciences.2019; 20(16): 3934.     CrossRef
    • A review on the role of M2 macrophages in bladder cancer; pathophysiology and targeting
      Laleh Sharifi, Mohammad Reza Nowroozi, Erfan Amini, Masoumeh Kourosh Arami, Mohsen Ayati, Monireh Mohsenzadegan
      International Immunopharmacology.2019; 76: 105880.     CrossRef
    • Tumor-associated macrophage infiltration in meningioma
      Dustin T Proctor, Jordan Huang, Sanju Lama, Abdulrahman Albakr, Guido Van Marle, Garnette R Sutherland
      Neuro-Oncology Advances.2019;[Epub]     CrossRef
    • Immune and Inflammatory Cells in Thyroid Cancer Microenvironment
      Ferrari, Fallahi, Galdiero, Ruffilli, Elia, Ragusa, Paparo, Patrizio, Mazzi, Varricchi, Marone, Antonelli
      International Journal of Molecular Sciences.2019; 20(18): 4413.     CrossRef
    • Caveolin-2 deficiency induces a rapid anti-tumor immune response prior to regression of implanted murine lung carcinoma tumors
      Yajun Liu, Xiaoqiang Qi, Guangfu Li, Grzegorz Sowa
      Scientific Reports.2019;[Epub]     CrossRef
    • Paclitaxel Treatment and Proprotein Convertase 1/3 (PC1/3) Knockdown in Macrophages is a Promising Antiglioma Strategy as Revealed by Proteomics and Cytotoxicity Studies
      Marie Duhamel, Mélanie Rose, Franck Rodet, Adriana Natalia Murgoci, Lea Zografidou, Anne Régnier-Vigouroux, Fabien Vanden Abeele, Firas Kobeissy, Serge Nataf, Laurent Pays, Maxence Wisztorski, Dasa Cizkova, Isabelle Fournier, Michel Salzet
      Molecular & Cellular Proteomics.2018; 17(6): 1126.     CrossRef
    • Chloroquine and nanoparticle drug delivery: A promising combination
      Joe Pelt, Sara Busatto, Mauro Ferrari, E. Aubrey Thompson, Kabir Mody, Joy Wolfram
      Pharmacology & Therapeutics.2018; 191: 43.     CrossRef
    • Conditioned medium from stimulated macrophages inhibits growth but induces an inflammatory phenotype in breast cancer cells
      Wenzhe Song, Parth Thakor, David A. Vesey, Glenda C. Gobe, Christudas Morais
      Biomedicine & Pharmacotherapy.2018; 106: 247.     CrossRef
    • Potential involvement of neutrophils in human thyroid cancer
      Maria Rosaria Galdiero, Gilda Varricchi, Stefania Loffredo, Claudio Bellevicine, Tiziana Lansione, Anne Lise Ferrara, Raffaella Iannone, Sarah di Somma, Francesco Borriello, Eduardo Clery, Maria Triassi, Giancarlo Troncone, Gianni Marone, Fabrizio Mattei
      PLOS ONE.2018; 13(6): e0199740.     CrossRef
    • CSF1R-Expressing Tumor-Associated Macrophages, Smoking and Survival in Lung Adenocarcinoma: Analyses Using Quantitative Phosphor-Integrated Dot Staining
      Kentaro Inamura, Yasuyuki Shigematsu, Hironori Ninomiya, Yasuhiro Nakashima, Maki Kobayashi, Haruyuki Saito, Katsuhiro Takahashi, Etsuko Futaya, Sakae Okumura, Yuichi Ishikawa, Hiroaki Kanda
      Cancers.2018; 10(8): 252.     CrossRef
    • Tumor heterogeneity and nanoparticle-mediated tumor targeting: the importance of delivery system personalization
      K. Laxmi Swetha, Aniruddha Roy
      Drug Delivery and Translational Research.2018; 8(5): 1508.     CrossRef
    • Immune Gene Signature Delineates a Subclass of Papillary Thyroid Cancer with Unfavorable Clinical Outcomes
      Kyuryung Kim, Sora Jeon, Tae-Min Kim, Chan Jung
      Cancers.2018; 10(12): 494.     CrossRef
    • Bone marrow-derived cells are recruited by the melanoma tumor with endothelial cells contributing to tumor vasculature
      R. Bonfim-Silva, L. E. B. Souza, F. U. F. Melo, V. C. Oliveira, D. A. R. Magalhães, H. F. Oliveira, D. T. Covas, A. M. Fontes
      Clinical and Translational Oncology.2017; 19(1): 125.     CrossRef
    • Stromal contributions to the carcinogenic process
      Mark Spaw, Shrikant Anant, Sufi Mary Thomas
      Molecular Carcinogenesis.2017; 56(4): 1199.     CrossRef
    • The Role of Cancer-Associated Fibroblasts and Fibrosis in Liver Cancer
      Silvia Affo, Le-Xing Yu, Robert F. Schwabe
      Annual Review of Pathology: Mechanisms of Disease.2017; 12(1): 153.     CrossRef
    • PEDF increases the tumoricidal activity of macrophages towards prostate cancer cells in vitro
      Dalia Martinez-Marin, Courtney Jarvis, Thomas Nelius, Werner de Riese, Olga V. Volpert, Stéphanie Filleur, Chih-Hsin Tang
      PLOS ONE.2017; 12(4): e0174968.     CrossRef
    • Anaplastic thyroid carcinoma: from clinicopathology to genetics and advanced therapies
      Eleonora Molinaro, Cristina Romei, Agnese Biagini, Elena Sabini, Laura Agate, Salvatore Mazzeo, Gabriele Materazzi, Stefano Sellari-Franceschini, Alessandro Ribechini, Liborio Torregrossa, Fulvio Basolo, Paolo Vitti, Rossella Elisei
      Nature Reviews Endocrinology.2017; 13(11): 644.     CrossRef
    • Iron Induces Anti-tumor Activity in Tumor-Associated Macrophages
      Milene Costa da Silva, Michael O. Breckwoldt, Francesca Vinchi, Margareta P. Correia, Ana Stojanovic, Carl Maximilian Thielmann, Michael Meister, Thomas Muley, Arne Warth, Michael Platten, Matthias W. Hentze, Adelheid Cerwenka, Martina U. Muckenthaler
      Frontiers in Immunology.2017;[Epub]     CrossRef
    • Reprogramming Tumor-Associated Macrophages To Reverse EGFRT790M Resistance by Dual-Targeting Codelivery of Gefitinib/Vorinostat
      Huige Peng, Binfan Chen, Wei Huang, Yubo Tang, Yifan Jiang, Wenyuan Zhang, Yongzhuo Huang
      Nano Letters.2017; 17(12): 7684.     CrossRef
    • Numerical modeling of nanodrug distribution in tumors with heterogeneous vasculature
      Cheng-Ying Chou, Wan-I Chang, Tzyy-Leng Horng, Win-Li Lin, Han-Chung Wu
      PLOS ONE.2017; 12(12): e0189802.     CrossRef
    • HPMA–Copolymer Nanocarrier Targets Tumor-Associated Macrophages in Primary and Metastatic Breast Cancer
      Melissa N. Zimel, Chloe B. Horowitz, Vinagolu K. Rajasekhar, Alexander B. Christ, Xin Wei, Jianbo Wu, Paulina M. Wojnarowicz, Dong Wang, Steven R. Goldring, P. Edward Purdue, John H. Healey
      Molecular Cancer Therapeutics.2017; 16(12): 2701.     CrossRef
    • Correlation of tumor-associated macrophages and NK cells with bladder cancer size and T stage in patients with solitary low-grade urothelial carcinoma
      Kristian Krpina, Emina Babarović, Josip Španjol, Gordana Đorđević, Tobias Maurer, Nives Jonjić
      Wiener klinische Wochenschrift.2016; 128(7-8): 248.     CrossRef
    • The lymphatic system and pancreatic cancer
      Darci M. Fink, Maria M. Steele, Michael A. Hollingsworth
      Cancer Letters.2016; 381(1): 217.     CrossRef
    • Jacalin-Activated Macrophages Exhibit an Antitumor Phenotype
      Cláudia Danella Polli, Luciana Pereira Ruas, Luciana Chain Veronez, Thais Herrero Geraldino, Fabiana Rossetto de Morais, Maria Cristina Roque-Barreira, Gabriela Pereira-da-Silva
      BioMed Research International.2016; 2016: 1.     CrossRef
    • The immune network in thyroid cancer
      Maria Rosaria Galdiero, Gilda Varricchi, Gianni Marone
      OncoImmunology.2016; 5(6): e1168556.     CrossRef
    • The Expression and Relationship of CD68-Tumor-Associated Macrophages and Microvascular Density With the Prognosis of Patients With Laryngeal Squamous Cell Carcinoma
      Shujun Sun, Xinliang Pan, Limin Zhao, Jianming Zhou, Hongzeng Wang, Yonghong Sun
      Clinical and Experimental Otorhinolaryngology.2016; 9(3): 270.     CrossRef
    • Role of pulmonary macrophages in initiation of lung metastasis in anaplastic thyroid cancer
      Xiu Juan Li, Prakash Gangadaran, Senthilkumar Kalimuthu, Ji Min Oh, Liya Zhu, Shin Young Jeong, Sang-Woo Lee, Jaetae Lee, Byeong-Cheol Ahn
      International Journal of Cancer.2016; 139(11): 2583.     CrossRef
    • Perspectives for immunotherapy in endocrine cancer
      S Latteyer, V Tiedje, B Schilling, D Führer
      Endocrine-Related Cancer.2016; 23(10): R469.     CrossRef
    • Macrophage Densities Correlated with CXC Chemokine Receptor 4 Expression and Related with Poor Survival in Anaplastic Thyroid Cancer
      Dae In Kim, Eunyoung Kim, Young A Kim, Sun Wook Cho, Jung Ah Lim, Young Joo Park
      Endocrinology and Metabolism.2016; 31(3): 469.     CrossRef
    • High expression of C-C chemokine receptor 2 associates with poor overall survival in gastric cancer patients after surgical resection
      Ruochen Li, Heng Zhang, Hao Liu, Chao Lin, Yifan Cao, Weijuan Zhang, Zhenbin Shen, Jiejie Xu
      Oncotarget.2016; 7(17): 23909.     CrossRef
    • Polycationic carbosilane dendrimer decreases angiogenesis and tumor-associated macrophages in tumor-bearing mice
      Ana Judith Perisé-Barrios, María Jesús Serramia, Javier de la Mata, Rafael Gomez, Angel Luis Corbí, Ángeles Domínguez-Soto, María Ángeles Muñoz-Fernandez
      RSC Advances.2015; 5(126): 104110.     CrossRef

    Figure

    JPTM : Journal of Pathology and Translational Medicine