Beyond tumor‑associated macrophages involved in spheroid formation and dissemination: Novel insights for ovarian cancer therapy (Review)
- Authors:
- Yuchen Liu
- Haoyue Xiao
- Hai Zeng
- Ying Xiang
-
Affiliations: Laboratory of Oncology, Center for Molecular Medicine, School of Basic Medicine, Health Science Center, Yangtze University, Jingzhou, Hubei 434023, P.R. China, Department of Oncology, First Affiliated Hospital of Yangtze University, Jingzhou, Hubei 434023, P.R. China - Published online on: November 7, 2024 https://doi.org/10.3892/ijo.2024.5705
- Article Number: 117
-
Copyright : © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
This article is mentioned in:
Abstract
 |
 |
 |
|
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Bast RC, Han CY, Lu Z and Lu KH: Next steps in the early detection of ovarian cancer. Commun Med (Lond). 1:362021. View Article : Google Scholar : PubMed/NCBI | |
|
Yang L, Xie HJ, Li YY, Wang X, Liu XX and Mai J: Molecular mechanisms of platinum-based chemotherapy resistance in ovarian cancer (review). Oncol Rep. 47:822022. View Article : Google Scholar | |
|
Almeida-Nunes DL, Mendes-Frias A, Silvestre R, Dinis-Oliveira RJ and Ricardo S: Immune tumor microenvironment in ovarian cancer ascites. Int J Mol Sci. 23:106922022. View Article : Google Scholar : PubMed/NCBI | |
|
Huang H, Li YJ, Lan CY, Huang QD, Feng YL, Huang YW and Liu JH: Clinical significance of ascites in epithelial ovarian cancer. Neoplasma. 60:546–552. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kim S, Kim B and Song YS: Ascites modulates cancer cell behavior, contributing to tumor heterogeneity in ovarian cancer. Cancer Sci. 107:1173–1178. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Quan Q, Zhou S, Liu Y, Yin W, Liao Q, Ren S, Zhang F, Meng Y and Mu X: Relationship between ascites volume and clinical outcomes in epithelial ovarian cancer. J Obstet Gynaecol Res. 47:1527–1535. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Cavazzoni E, Bugiantella W, Graziosi L, Franceschini MS and Donini A: Malignant ascites: Pathophysiology and treatment. Int J Clin Oncol. 18:1–9. 2013. View Article : Google Scholar | |
|
Yeung TL, Leung CS, Yip KP, Au Yeung CL, Wong ST and Mok SC: Cellular and molecular processes in ovarian cancer metastasis. A review in the theme: Cell and molecular processes in cancer metastasis. Am J Physiol Cell Physiol. 309:C444–C456. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Al Habyan S, Kalos C, Szymborski J and McCaffrey L: Multicellular detachment generates metastatic spheroids during intra-abdominal dissemination in epithelial ovarian cancer. Oncogene. 37:5127–5135. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ahmed N and Stenvers KL: Getting to know ovarian cancer ascites: Opportunities for targeted therapy-based translational research. Front Oncol. 3:2562013. View Article : Google Scholar : PubMed/NCBI | |
|
Dhaliwal D and Shepherd TG: Molecular and cellular mechanisms controlling integrin-mediated cell adhesion and tumor progression in ovarian cancer metastasis: A review. Clin Exp Metastasis. 39:291–301. 2022. View Article : Google Scholar : | |
|
Worzfeld T, Pogge von Strandmann E, Huber M, Adhikary T, Wagner U, Reinartz S and Müller R: The unique molecular and cellular microenvironment of ovarian cancer. Front Oncol. 7:242017. View Article : Google Scholar : PubMed/NCBI | |
|
Gao Q, Yang Z, Xu S, Li X, Yang X, Jin P, Liu Y, Zhou X, Zhang T, Gong C, et al: Heterotypic CAF-tumor spheroids promote early peritoneal metastatis of ovarian cancer. J Exp Med. 216:688–703. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Pan Y, Yu Y, Wang X and Zhang T: Tumor-associated macrophages in tumor immunity. Front Immunol. 11:5830842020. View Article : Google Scholar : PubMed/NCBI | |
|
Long L, Hu Y, Long T, Lu X, Tuo Y, Li Y and Ke Z: Tumor-associated macrophages induced spheroid formation by CCL18-ZEB1-M-CSF feedback loop to promote transcoelomic metastasis of ovarian cancer. J Immunother Cancer. 9:e0039732021. View Article : Google Scholar | |
|
Yin M, Li X, Tan S, Zhou HJ, Ji W, Bellone S, Xu X, Zhang H, Santin AD, Lou G and Min W: Tumor-associated macrophages drive spheroid formation during early transcoelomic metastasis of ovarian cancer. J Clin Invest. 126:4157–4173. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Song M, Yeku OO, Rafiq S, Purdon T, Dong X, Zhu L, Zhang T, Wang H, Yu Z, Mai J, et al: Tumor derived UBR5 promotes ovarian cancer growth and metastasis through inducing immunosuppressive macrophages. Nat Commun. 11:62982020. View Article : Google Scholar : PubMed/NCBI | |
|
El-Arabey AA, Alkhalil SS, Al-Shouli ST, Awadalla ME, Alhamdi HW, Almanaa TN, Mohamed SSEM and Abdalla M: Revisiting macrophages in ovarian cancer microenvironment: Development, function and interaction. Med Oncol. 40:1422023. View Article : Google Scholar : PubMed/NCBI | |
|
Larionova I, Tuguzbaeva G, Ponomaryova A, Stakheyeva M, Cherdyntseva N, Pavlov V, Choinzonov E and Kzhyshkowska J: Tumor-associated macrophages in human breast, colorectal, lung, ovarian and prostate cancers. Front Oncol. 10:5665112020. View Article : Google Scholar : PubMed/NCBI | |
|
Miyamoto T, Murphy B and Zhang N: Intraperitoneal metastasis of ovarian cancer: New insights on resident macrophages in the peritoneal cavity. Front Immunol. 14:11046942023. View Article : Google Scholar : PubMed/NCBI | |
|
Yin M, Shen J, Yu S, Fei J, Zhu X, Zhao J, Zhai L, Sadhukhan A and Zhou J: Tumor-associated macrophages (TAMs): A critical activator in ovarian cancer metastasis. Onco Targets Ther. 12:8687–8699. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Jazwinska DE, Kulawiec DG and Zervantonakis IK: Cancer-mesothelial and cancer-macrophage interactions in the ovarian cancer microenvironment. Am J Physiol Cell Physiol. 325:C721–C730. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Klymenko Y, Johnson J, Bos B, Lombard R, Campbell L, Loughran E and Stack MS: Heterogeneous cadherin expression and multicellular aggregate dynamics in ovarian cancer dissemination. Neoplasia. 19:549–563. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ford CE, Werner B, Hacker NF and Warton K: The untapped potential of ascites in ovarian cancer research and treatment. Br J Cancer. 123:9–16. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Habanjar O, Diab-Assaf M, Caldefie-Chezet F and Delort L: 3D cell culture systems: Tumor application, advantages, and disadvantages. Int J Mol Sci. 22:122002021. View Article : Google Scholar : PubMed/NCBI | |
|
Matte I, Legault CM, Garde-Granger P, Laplante C, Bessette P, Rancourt C and Piché A: Mesothelial cells interact with tumor cells for the formation of ovarian cancer multicellular spheroids in peritoneal effusions. Clin Exp Metastasis. 33:839–852. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Xu S, Yang Y, Dong L, Qiu W, Yang L, Wang X and Liu L: Construction and characteristics of an E-cadherin-related three-dimensional suspension growth model of ovarian cancer. Sci Rep. 4:56462014. View Article : Google Scholar : PubMed/NCBI | |
|
Sawada K, Mitra AK, Radjabi AR, Bhaskar V, Kistner EO, Tretiakova M, Jagadeeswaran S, Montag A, Becker A, Kenny HA, et al: Loss of E-cadherin promotes ovarian cancer metastasis via alpha 5-integrin, which is a therapeutic target. Cancer Res. 68:2329–2339. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Casey RC, Burleson KM, Skubitz KM, Pambuccian SE, Oegema TR Jr, Ruff LE and Skubitz AP: Beta 1-integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids. Am J Pathol. 159:2071–2080. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Han Q, Huang B, Huang Z, Cai J, Gong L, Zhang Y, Jiang J, Dong W and Wang Z: Tumor cell-fibroblast heterotypic aggregates in malignant ascites of patients with ovarian cancer. Int J Mol Med. 44:2245–2255. 2019.PubMed/NCBI | |
|
Hassn Mesrati M, Syafruddin SE, Mohtar MA and Syahir A: CD44: A multifunctional mediator of cancer progression. Biomolecules. 11:18502021. View Article : Google Scholar : PubMed/NCBI | |
|
Chen MW, Yang ST, Chien MH, Hua KT, Wu CJ, Hsiao SM, Lin H, Hsiao M, Su JL and Wei LH: The STAT3-miRNA-92-Wnt signaling pathway regulates spheroid formation and malignant progression in ovarian cancer. Cancer Res. 77:1955–1967. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li SS, Ma J and Wong AST: Chemoresistance in ovarian cancer: Exploiting cancer stem cell metabolism. J Gynecol Oncol. 29:e322018. View Article : Google Scholar : PubMed/NCBI | |
|
Casagrande N, Borghese C, Agostini F, Durante C, Mazzucato M, Colombatti A and Aldinucci D: In ovarian cancer multicellular spheroids, platelet releasate promotes growth, expansion of ALDH+ and CD133+ cancer stem cells, and protection against the cytotoxic effects of cisplatin, carboplatin and paclitaxel. Int J Mol Sci. 22:30192021. View Article : Google Scholar : PubMed/NCBI | |
|
Condello S, Morgan CA, Nagdas S, Cao L, Turek J, Hurley TD and Matei D: β-Catenin-regulated ALDH1A1 is a target in ovarian cancer spheroids. Oncogene. 34:2297–2308. 2015. View Article : Google Scholar | |
|
Cui TX, Kryczek I, Zhao L, Zhao E, Kuick R, Roh MH, Vatan L, Szeliga W, Mao Y, Thomas DG, et al: Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity. 39:611–621. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Suganuma T, Ino K, Shibata K, Kajiyama H, Nagasaka T, Mizutani S and Kikkawa F: Functional expression of the angiotensin II type 1 receptor in human ovarian carcinoma cells and its blockade therapy resulting in suppression of tumor invasion, angiogenesis, and peritoneal dissemination. Clin Cancer Res. 11:2686–2694. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Q, Yu S, Lam MMT, Poon TCW, Sun L, Jiao Y, Wong AST and Lee LTO: Angiotensin II promotes ovarian cancer spheroid formation and metastasis by upregulation of lipid desaturation and suppression of endoplasmic reticulum stress. J Exp Clin Cancer Res. 38:1162019. View Article : Google Scholar : PubMed/NCBI | |
|
Adeshakin FO, Adeshakin AO, Afolabi LO, Yan D, Zhang G and Wan X: Mechanisms for modulating anoikis resistance in cancer and the relevance of metabolic reprogramming. Front Oncol. 11:6265772021. View Article : Google Scholar : PubMed/NCBI | |
|
Frisch SM and Screaton RA: Anoikis mechanisms. Curr Opin Cell Biol. 13:555–562. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Grossmann J: Molecular mechanisms of 'detachment-induced apoptosis-Anoikis'. Apoptosis. 7:247–260. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Taddei ML, Giannoni E, Fiaschi T and Chiarugi P: Anoikis: An emerging hallmark in health and diseases. J Pathol. 226:380–393. 2012. View Article : Google Scholar | |
|
Cai Q, Yan L and Xu Y: Anoikis resistance is a critical feature of highly aggressive ovarian cancer cells. Oncogene. 34:3315–3324. 2015. View Article : Google Scholar : | |
|
Cancer Genome Atlas Research Network: Integrated genomic analyses of ovarian carcinoma. Nature. 474:609–615. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Park JT, Shih IeM and Wang TL: Identification of Pbx1, a potential oncogene, as a Notch3 target gene in ovarian cancer. Cancer Res. 68:8852–8860. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Brown CW, Brodsky AS and Freiman RN: Notch3 overexpression promotes anoikis resistance in epithelial ovarian cancer via upregulation of COL4A2. Mol Cancer Res. 13:78–85. 2015. View Article : Google Scholar : | |
|
Tang MKS, Zhou HY, Yam JW and Wong AS: c-Met overexpression contributes to the acquired apoptotic resistance of nonadherent ovarian cancer cells through a cross talk mediated by phosphatidylinositol 3-kinase and extracellular signal-regulated kinase 1/2. Neoplasia. 12:128–138. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Lopez A, Reyna DE, Gitego N, Kopp F, Zhou H, Miranda-Roman MA, Nordstrøm LU, Narayanagari SR, Chi P, Vilar E, et al: Co-targeting of BAX and BCL-XL proteins broadly overcomes resistance to apoptosis in cancer. Nat Commun. 13:11992022. View Article : Google Scholar : PubMed/NCBI | |
|
Mei H, Nakatsu MN, Baclagon ER and Deng SX: Frizzled 7 maintains the undifferentiated state of human limbal stem/progenitor cells. Stem Cells. 32:938–945. 2014. View Article : Google Scholar | |
|
Condello S, Sima L, Ivan C, Cardenas H, Schiltz G, Mishra RK and Matei D: Tissue tranglutaminase regulates interactions between ovarian cancer stem cells and the tumor niche. Cancer Res. 78:2990–3001. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Qin Q, Xu Y, He T, Qin C and Xu J: Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms. Cell Res. 22:90–106. 2012. View Article : Google Scholar : | |
|
Tan M, Asad M, Heong V, Wong MK, Tan TZ, Ye J, Kuay KT, Thiery JP, Scott C and Huang RY: The FZD7-TWIST1 axis is responsible for anoikis resistance and tumorigenesis in ovarian carcinoma. Mol Oncol. 13:757–780. 2019. View Article : Google Scholar : | |
|
Motohara T, Masuda K, Morotti M, Zheng Y, El-Sahhar S, Chong KY, Wietek N, Alsaadi A, Carrami EM, Hu Z, et al: An evolving story of the metastatic voyage of ovarian cancer cells: Cellular and molecular orchestration of the adipose-rich metastatic microenvironment. Oncogene. 38:2885–2898. 2019. View Article : Google Scholar : | |
|
Dai ZY, Jin SM, Luo HQ, Leng HL and Fang JD: LncRNA HOTAIR regulates anoikis-resistance capacity and spheroid formation of ovarian cancer cells by recruiting EZH2 and influencing H3K27 methylation. Neoplasma. 68:509–518. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang L, Huang J, Yang N, Greshock J, Liang S, Hasegawa K, Giannakakis A, Poulos N, O'Brien-Jenkins A, Katsaros D, et al: Integrative genomic analysis of phosphatidylinositol 3′-kinase family identifies PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clin Cancer Res. 13:5314–5321. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Dong L and Hui L: HOTAIR promotes proliferation, migration, and invasion of ovarian cancer SKOV3 cells through regulating PIK3R3. Med Sci Monit. 22:325–331. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Dolinschek R, Hingerl J, Benge A, Zafiu C, Schüren E, Ehmoser EK, Lössner D and Reuning U: Constitutive activation of integrin αvβ3 contributes to anoikis resistance of ovarian cancer cells. Mol Oncol. 15:503–522. 2021. View Article : Google Scholar | |
|
Yu X, Liu L, Cai B, He Y and Wan X: Suppression of anoikis by the neurotrophic receptor TrkB in human ovarian cancer. Cancer Sci. 99:543–552. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Carduner L, Picot CR, Leroy-Dudal J, Blay L, Kellouche S and Carreiras F: Cell cycle arrest or survival signaling through αv integrins, activation of PKC and ERK1/2 lead to anoikis resistance of ovarian cancer spheroids. Exp Cell Res. 320:329–342. 2014. View Article : Google Scholar | |
|
Kim S, Kim S, Kim J, Kim B, Kim SI, Kim MA, Kwon S and Song YS: Evaluating tumor evolution via genomic profiling of individual tumor spheroids in a malignant ascites. Sci Rep. 8:127242018. View Article : Google Scholar : PubMed/NCBI | |
|
Allen HJ, Porter C, Gamarra M, Piver MS and Johnson EA: Isolation and morphologic characterization of human ovarian carcinoma cell clusters present in effusions. Exp Cell Biol. 55:194–208. 1987.PubMed/NCBI | |
|
Azharuddin M, Roberg K, Dhara AK, Jain MV, Darcy P, Hinkula J, Slater NKH and Patra HK: Dissecting multi drug resistance in head and neck cancer cells using multicellular tumor spheroids. Sci Rep. 9:200662019. View Article : Google Scholar : PubMed/NCBI | |
|
Świerczewska M, Sterzyńska K, Ruciński M, Andrzejewska M, Nowicki M and Januchowski R: The response and resistance to drugs in ovarian cancer cell lines in 2D monolayers and 3D spheroids. Biomed Pharmacother. 165:1151522023. View Article : Google Scholar : PubMed/NCBI | |
|
Sun Y, Li S, Yang L, Zhang D, Zhao Z, Gao J and Liu L: CDC25A facilitates chemo-resistance in ovarian cancer multicellular spheroids by promoting E-cadherin expression and arresting cell cycles. J Cancer. 10:2874–2884. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Shen T and Huang S: The role of Cdc25A in the regulation of cell proliferation and apoptosis. Anticancer Agents Med Chem. 12:631–639. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Broggini M, Buraggi G, Brenna A, Riva L, Codegoni AM, Torri V, Lissoni AA, Mangioni C and D'Incalci M: Cell cycle-related phosphatases CDC25A and B expression correlates with survival in ovarian cancer patients. Anticancer Res. 20:4835–4840. 2000. | |
|
Green SK, Francia G, Isidoro C and Kerbel RS: Antiadhesive antibodies targeting E-cadherin sensitize multicellular tumor spheroids to chemotherapy in vitro. Mol Cancer Ther. 3:149–159. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Lim GH, An JH, Park SM, Youn GH, Oh YI, Seo KW and Youn HY: Macrophage induces anti-cancer drug resistance in canine mammary gland tumor spheroid. Sci Rep. 13:103942023. View Article : Google Scholar : PubMed/NCBI | |
|
Makhija S, Taylor DD, Gibb RK and Gerçel-Taylor C: Taxol-induced bcl-2 phosphorylation in ovarian cancer cell monolayer and spheroids. Int J Oncol. 14:515–521. 1999.PubMed/NCBI | |
|
Yvon AM, Wadsworth P and Jordan MA: Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell. 10:947–959. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Makovec T: Cisplatin and beyond: Molecular mechanisms of action and drug resistance development in cancer chemotherapy. Radiol Oncol. 53:148–158. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Kwon MJ and Shin YK: Regulation of ovarian cancer stem cells or tumor-initiating cells. Int J Mol Sci. 14:6624–6648. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Liao J, Qian F, Tchabo N, Mhawech-Fauceglia P, Beck A, Qian Z, Wang X, Huss WJ, Lele SB, Morrison CD and Odunsi K: Ovarian cancer spheroid cells with stem cell-like properties contribute to tumor generation, metastasis and chemotherapy resistance through hypoxia-resistant metabolism. PLoS One. 9:e849412014. View Article : Google Scholar : PubMed/NCBI | |
|
McAuliffe SM, Morgan SL, Wyant GA, Tran LT, Muto KW, Chen YS, Chin KT, Partridge JC, Poole BB, Cheng KH, et al: Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proc Natl Acad Sci USA. 109:E2939–E2948. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kang H, Jeong JY, Song JY, Kim TH, Kim G, Huh JH, Kwon AY, Jung SG and An HJ: Notch3-specific inhibition using siRNA knockdown or GSI sensitizes paclitaxel-resistant ovarian cancer cells. Mol Carcinog. 55:1196–1209. 2016. View Article : Google Scholar | |
|
van Baal JOAM, Van de Vijver KK, Nieuwland R, van Noorden CJF, van Driel WJ, Sturk A, Kenter GG, Rikkert LG and Lok CAR: The histophysiology and pathophysiology of the peritoneum. Tissue Cell. 49:95–105. 2017. View Article : Google Scholar | |
|
Nakamura M, Ono YJ, Kanemura M, Tanaka T, Hayashi M, Terai Y and Ohmichi M: Hepatocyte growth factor secreted by ovarian cancer cells stimulates peritoneal implantation via the mesothelial-mesenchymal transition of the peritoneum. Gynecol Oncol. 139:345–354. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yousefi M, Dehghani S, Nosrati R, Ghanei M, Salmaninejad A, Rajaie S, Hasanzadeh M and Pasdar A: Current insights into the metastasis of epithelial ovarian cancer-hopes and hurdles. Cell Oncol (Dordr). 43:515–538. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Cui L, Johkura K, Liang Y, Teng R, Ogiwara N, Okouchi Y, Asanuma K and Sasaki K: Biodefense function of omental milky spots through cell adhesion molecules and leukocyte proliferation. Cell Tissue Res. 310:321–330. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Niedbala MJ, Crickard K and Bernacki RJ: Interactions of human ovarian tumor cells with human mesothelial cells grown on extracellular matrix. An in vitro model system for studying tumor cell adhesion and invasion. Exp Cell Res. 160:499–513. 1985. View Article : Google Scholar : PubMed/NCBI | |
|
Iwanicki MP, Davidowitz RA, Ng MR, Besser A, Muranen T, Merritt M, Danuser G, Ince TA and Brugge JS: Ovarian cancer spheroids use myosin-generated force to clear the mesothelium. Cancer Discov. 1:144–157. 2011. View Article : Google Scholar | |
|
Cannistra SA, Kansas GS, Niloff J, DeFranzo B, Kim Y and Ottensmeier C: Binding of ovarian cancer cells to peritoneal mesothelium in vitro is partly mediated by CD44H. Cancer Res. 53:3830–3838. 1993.PubMed/NCBI | |
|
Witz CA, Montoya-Rodriguez IA, Cho S, Centonze VE, Bonewald LF and Schenken RS: Composition of the extracellular matrix of the peritoneum. J Soc Gynecol Investig. 8:299–304. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Burleson KM, Casey RC, Skubitz KM, Pambuccian SE, Oegema TR Jr and Skubitz AP: Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers. Gynecol Oncol. 93:170–181. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Burleson KM, Boente MP, Pambuccian SE and Skubitz AP: Disaggregation and invasion of ovarian carcinoma ascites spheroids. J Transl Med. 4:62006. View Article : Google Scholar : PubMed/NCBI | |
|
Moser TL, Pizzo SV, Bafetti LM, Fishman DA and Stack MS: Evidence for preferential adhesion of ovarian epithelial carcinoma cells to type I collagen mediated by the alpha2beta1 integrin. Int J Cancer. 67:695–701. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Shield K, Riley C, Quinn MA, Rice GE, Ackland ML and Ahmed N: Alpha2beta1 integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis. J Carcinog. 6:112007. View Article : Google Scholar : PubMed/NCBI | |
|
Gupta V, Yull F and Khabele D: Bipolar tumor-associated macrophages in ovarian cancer as targets for therapy. Cancers (Basel). 10:3662018. View Article : Google Scholar : PubMed/NCBI | |
|
Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J and Harris AL: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56:4625–4629. 1996.PubMed/NCBI | |
|
Lewis JS, Landers RJ, Underwood JC, Harris AL and Lewis CE: Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol. 192:150–158. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Shibuya M: Vascular endothelial growth factor and its receptor system: Physiological functions in angiogenesis and pathological roles in various diseases. J Biochem. 153:13–19. 2013. View Article : Google Scholar | |
|
Han KY, Kim CW, Lee TH, Son Y and Kim J: CCL23 up-regulates expression of KDR/Flk-1 and potentiates VEGF-induced proliferation and migration of human endothelial cells. Biochem Biophys Res Commun. 382:124–128. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hefler LA, Zeillinger R, Grimm C, Sood AK, Cheng WF, Gadducci A, Tempfer CB and Reinthaller A: Preoperative serum vascular endothelial growth factor as a prognostic parameter in ovarian cancer. Gynecol Oncol. 103:512–517. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Byrne AT, Ross L, Holash J, Nakanishi M, Hu L, Hofmann JI, Yancopoulos GD and Jaffe RB: Vascular endothelial growth factor-trap decreases tumor burden, inhibits ascites, and causes dramatic vascular remodeling in an ovarian cancer model. Clin Cancer Res. 9:5721–5728. 2003.PubMed/NCBI | |
|
Jeon BH, Jang C, Han J, Kataru RP, Piao L, Jung K, Cha HJ, Schwendener RA, Jang KY, Kim KS, et al: Profound but dysfunctional lymphangiogenesis via vascular endothelial growth factor ligands from CD11b+ macrophages in advanced ovarian cancer. Cancer Res. 68:1100–1109. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang S, Xie B, Wang L, Yang H, Zhang H, Chen Y, Wang F, Liu C and He H: Macrophage-mediated vascular permeability via VLA4/VCAM1 pathway dictates ascites development in ovarian cancer. J Clin Invest. 131:e1403152021. View Article : Google Scholar : | |
|
Reinartz S, Schumann T, Finkernagel F, Wortmann A, Jansen JM, Meissner W, Krause M, Schwörer AM, Wagner U, Müller-Brüsselbach S and Müller R: Mixed-polarization phenotype of ascites-associated macrophages in human ovarian carcinoma: Correlation of CD163 expression, cytokine levels and early relapse. Int J Cancer. 134:32–42. 2014. View Article : Google Scholar : | |
|
Moughon DL, He H, Schokrpur S, Jiang ZK, Yaqoob M, David J, Lin C, Iruela-Arispe ML, Dorigo O and Wu L: Macrophage blockade using CSF1R inhibitors reverses the vascular leakage underlying malignant ascites in late-stage epithelial ovarian cancer. Cancer Res. 75:4742–4752. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Clancy JL, Henderson MJ, Russell AJ, Anderson DW, Bova RJ, Campbell IG, Choong DY, Macdonald GA, Mann GJ, Nolan T, et al: EDD, the human orthologue of the hyperplastic discs tumour suppressor gene, is amplified and overexpressed in cancer. Oncogene. 22:5070–5081. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Shearer RF, Iconomou M, Watts CK and Saunders DN: Functional roles of the E3 ubiquitin ligase UBR5 in cancer. Mol Cancer Res. 13:1523–1532. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Tang M, Liu B, Bu X and Zhao P: Cross-talk between ovarian cancer cells and macrophages through periostin promotes macrophage recruitment. Cancer Sci. 109:1309–1318. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Durlanik S, Fundel-Clemens K, Viollet C, Huber HJ, Lenter M, Kitt K and Pflanz S: CD276 is an important player in macrophage recruitment into the tumor and an upstream regulator for PAI-1. Sci Rep. 11:148492021. View Article : Google Scholar : PubMed/NCBI | |
|
Worzfeld T, Finkernagel F, Reinartz S, Konzer A, Adhikary T, Nist A, Stiewe T, Wagner U, Looso M, Graumann J and Müller R: Proteotranscriptomics reveal signaling networks in the ovarian cancer microenvironment. Mol Cell Proteomics. 17:270–289. 2018. View Article : Google Scholar : | |
|
Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K and Gotoh Y: Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 275:90–94. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Yin M, Zhou HJ, Zhang J, Lin C, Li H, Li X, Li Y, Zhang H, Breckenridge DG, Ji W and Min W: ASK1-dependent endothelial cell activation is critical in ovarian cancer growth and metastasis. JCI Insight. 2:e918282017. View Article : Google Scholar : PubMed/NCBI | |
|
Sica A and Mantovani A: Macrophage plasticity and polarization: In vivo veritas. J Clin Invest. 122:787–795. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Mills CD, Kincaid K, Alt JM, Heilman MJ and Hill AM: M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol. 164:6166–6173. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Mantovani A, Sozzani S, Locati M, Allavena P and Sica A: Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23:549–555. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A and Locati M: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677–686. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Wen Y and Crowley SD: The varying roles of macrophages in kidney injury and repair. Curr Opin Nephrol Hypertens. 29:286–292. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL, Coskran T, Black SC, Brees DJ, Wicks JR, et al: Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest. 112:197–208. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Gao J, Liang Y and Wang L: Shaping polarization of tumor-associated macrophages in cancer immunotherapy. Front Immunol. 13:8887132022. View Article : Google Scholar : PubMed/NCBI | |
|
Wan C, Sun Y, Tian Y, Lu L, Dai X, Meng J, Huang J, He Q, Wu B, Zhang Z, et al: Irradiated tumor cell-derived microparticles mediate tumor eradication via cell killing and immune reprogramming. Sci Adv. 6:eaay97892020. View Article : Google Scholar : PubMed/NCBI | |
|
Shu Y and Cheng P: Targeting tumor-associated macrophages for cancer immunotherapy. Biochim Biophys Acta Rev Cancer. 1874:1884342020. View Article : Google Scholar : PubMed/NCBI | |
|
He J, Yin P and Xu K: Effect and molecular mechanisms of traditional Chinese medicine on tumor targeting tumor-associated macrophages. Drug Des Devel Ther. 14:907–919. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Macciò A, Gramignano G, Cherchi MC, Tanca L, Melis L and Madeddu C: Role of M1-polarized tumor-associated macrophages in the prognosis of advanced ovarian cancer patients. Sci Rep. 10:60962020. View Article : Google Scholar : PubMed/NCBI | |
|
Guiducci C, Vicari AP, Sangaletti S, Trinchieri G and Colombo MP: Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 65:3437–3446. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Capellero S, Erriquez J, Battistini C, Porporato R, Scotto G, Borella F, Di Renzo MF, Valabrega G and Olivero M: Ovarian cancer cells in ascites form aggregates that display a hybrid epithelial-mesenchymal phenotype and allows survival and proliferation of metastasizing cells. Int J Mol Sci. 23:8332022. View Article : Google Scholar : PubMed/NCBI | |
|
Sun S, Pan X, Zhao L, Zhou J, Wang H and Sun Y: The expression and relationship of CD68-tumor-associated macrophages and microvascular density with the prognosis of patients with laryngeal squamous cell carcinoma. Clin Exp Otorhinolaryngol. 9:270–277. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Sadrkhanloo M, Entezari M, Orouei S, Ghollasi M, Fathi N, Rezaei S, Hejazi ES, Kakavand A, Saebfar H, Hashemi M, et al: STAT3-EMT axis in tumors: Modulation of cancer metastasis, stemness and therapy response. Pharmacol Res. 182:1063112022. View Article : Google Scholar : PubMed/NCBI | |
|
Liang R, Chen X, Chen L, Wan F, Chen K, Sun Y and Zhu X: STAT3 signaling in ovarian cancer: A potential therapeutic target. J Cancer. 11:837–848. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Takaishi K, Komohara Y, Tashiro H, Ohtake H, Nakagawa T, Katabuchi H and Takeya M: Involvement of M2-polarized macrophages in the ascites from advanced epithelial ovarian carcinoma in tumor progression via Stat3 activation. Cancer Sci. 101:2128–2136. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Jinushi M, Chiba S, Yoshiyama H, Masutomi K, Kinoshita I, Dosaka-Akita H, Yagita H, Takaoka A and Tahara H: Tumor-associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells. Proc Natl Acad Sci USA. 108:12425–12430. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Raghavan S, Mehta P, Xie Y, Lei YL and Mehta G: Ovarian cancer stem cells and macrophages reciprocally interact through the WNT pathway to promote pro-tumoral and malignant phenotypes in 3D engineered microenvironments. J Immunother Cancer. 7:1902019. View Article : Google Scholar : PubMed/NCBI | |
|
Ruffell B and Coussens LM: Macrophages and therapeutic resistance in cancer. Cancer Cell. 27:462–472. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Li L, He D, Guo Q, Zhang Z, Ru D, Wang L, Gong K, Liu F, Duan Y and Li H: Exosome-liposome hybrid nanoparticle codelivery of TP and miR497 conspicuously overcomes chemoresistant ovarian cancer. J Nanobiotechnology. 20:502022. View Article : Google Scholar : PubMed/NCBI | |
|
Li H, Luo F, Jiang X, Zhang W, Xiang T, Pan Q, Cai L, Zhao J, Weng D, Li Y, et al: CircITGB6 promotes ovarian cancer cisplatin resistance by resetting tumor-associated macrophage polarization toward the M2 phenotype. J Immunother Cancer. 10:e0040292022. View Article : Google Scholar : PubMed/NCBI | |
|
Ding L, Wang Q, Martincuks A, Kearns MJ, Jiang T, Lin Z, Cheng X, Qian C, Xie S, Kim HJ, et al: STING agonism overcomes STAT3-mediated immunosuppression and adaptive resistance to PARP inhibition in ovarian cancer. J Immunother Cancer. 11:e0056272023. View Article : Google Scholar : PubMed/NCBI | |
|
Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, Wang J, Contreras-Trujillo H, Martin R, Cohen JD, et al: The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci USA. 109:6662–6667. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sikic BI, Lakhani N, Patnaik A, Shah SA, Chandana SR, Rasco D, Colevas AD, O'Rourke T, Narayanan S, Papadopoulos K, et al: First-in-human, first-in-class phase I trial of the anti-CD47 antibody Hu5F9-G4 in patients with advanced cancers. J Clin Oncol. 37:946–953. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Huang Y, Lv SQ, Liu PY, Ye ZL, Yang H, Li LF, Zhu HL, Wang Y, Cui LZ, Jiang DQ, et al: A SIRPα-Fc fusion protein enhances the antitumor effect of oncolytic adenovirus against ovarian cancer. Mol Oncol. 14:657–668. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Batchu RB, Gruzdyn OV, Kolli BK, Dachepalli R, Umar PS, Rai SK, Singh N, Tavva PS, Weaver DW and Gruber SA: IL-10 signaling in the tumor microenvironment of ovarian cancer. Adv Exp Med Biol. 1290:51–65. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
McKarns SC, Schwartz RH and Kaminski NE: Smad3 is essential for TGF-beta 1 to suppress IL-2 production and TCR-induced proliferation, but not IL-2-induced proliferation. J Immunol. 172:4275–4284. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Wertel I, Surówka J, Polak G, Barczyński B, Bednarek W, Jakubowicz-Gil J, Bojarska-Junak A and Kotarski J: Macrophage-derived chemokine CCL22 and regulatory T cells in ovarian cancer patients. Tumour Biol. 36:4811–4817. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Kamat K, Krishnan V and Dorigo O: Macrophage-derived CCL23 upregulates expression of T-cell exhaustion markers in ovarian cancer. Br J Cancer. 127:1026–1033. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Noy R and Pollard JW: Tumor-associated macrophages: From mechanisms to therapy. Immunity. 41:49–61. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chapoval AI, Ni J, Lau JS, Wilcox RA, Flies DB, Liu D, Dong H, Sica GL, Zhu G, Tamada K and Chen L: B7-H3: A costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol. 2:269–274. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Miyamoto T, Murakami R, Hamanishi J, Tanigaki K, Hosoe Y, Mise N, Takamatsu S, Mise Y, Ukita M, Taki M, et al: B7-H3 suppresses antitumor immunity via the CCL2-CCR2-M2 macrophage axis and contributes to ovarian cancer progression. Cancer Immunol Res. 10:56–69. 2022. View Article : Google Scholar | |
|
Liu Z, Jin K, Zeng H, Shao F, Chang Y, Wang Y, Xu L, Wang Z, Cui X, Zhu Y and Xu J: B7-H4 correlates with clinical outcome and immunotherapeutic benefit in muscle-invasive bladder cancer. Eur J Cancer. 171:133–142. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, et al: B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med. 203:871–881. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Carroll MJ, Fogg KC, Patel HA, Krause HB, Mancha AS, Patankar MS, Weisman PS, Barroilhet L and Kreeger PK: Alternatively-activated macrophages upregulate mesothelial expression of P-selectin to enhance adhesion of ovarian cancer cells. Cancer Res. 78:3560–3573. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Robinson-Smith TM, Isaacsohn I, Mercer CA, Zhou M, Van Rooijen N, Husseinzadeh N, McFarland-Mancini MM and Drew AF: Macrophages mediate inflammation-enhanced metastasis of ovarian tumors in mice. Cancer Res. 67:5708–5716. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Fogg KC, Olson WR, Miller JN, Khan A, Renner C, Hale I, Weisman PS and Kreeger PK: Alternatively activated macrophage-derived secretome stimulates ovarian cancer spheroid spreading through a JAK2/STAT3 pathway. Cancer Lett. 458:92–101. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zeng XY, Xie H, Yuan J, Jiang XY, Yong JH, Zeng D, Dou YY and Xiao SS: M2-like tumor-associated macrophages-secreted EGF promotes epithelial ovarian cancer metastasis via activating EGFR-ERK signaling and suppressing lncRNA LIMT expression. Cancer Biol Ther. 20:956–966. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, Erba E, Uboldi S, Zucchetti M, Pasqualini F, et al: Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell. 23:249–262. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Sandhu SK, Papadopoulos K, Fong PC, Patnaik A, Messiou C, Olmos D, Wang G, Tromp BJ, Puchalski TA, Balkwill F, et al: A first-in-human, first-in-class, phase I study of carlumab (CNTO 888), a human monoclonal antibody against CC-chemokine ligand 2 in patients with solid tumors. Cancer Chemother Pharmacol. 71:1041–1050. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wesolowski R, Sharma N, Reebel L, Rodal MB, Peck A, West BL, Marimuthu A, Severson P, Karlin DA, Dowlati A, et al: Phase Ib study of the combination of pexidartinib (PLX3397), a CSF-1R inhibitor, and paclitaxel in patients with advanced solid tumors. Ther Adv Med Oncol. 11:17588359198542382019. View Article : Google Scholar : PubMed/NCBI | |
|
Zeng Y, Li B, Liang Y, Reeves PM, Qu X, Ran C, Liu Q, Callahan MV, Sluder AE, Gelfand JA, et al: Dual blockade of CXCL12-CXCR4 and PD-1-PD-L1 pathways prolongs survival of ovarian tumor-bearing mice by prevention of immunosuppression in the tumor microenvironment. FASEB J. 33:6596–6608. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Wanderley CW, Colón DF, Luiz JPM, Oliveira FF, Viacava PR, Leite CA, Pereira JA, Silva CM, Silva CR, Silva RL, et al: Paclitaxel reduces tumor growth by reprogramming tumor-associated macrophages to an M1 Profile in a TLR4-dependent manner. Cancer Res. 78:5891–5900. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Q, Li Y, Miao C, Wang Y, Xu Y, Dong R, Zhang Z, Griffin BB, Yuan C, Yan S, et al: Anti-angiogenesis effect of Neferine via regulating autophagy and polarization of tumor-associated macrophages in high-grade serous ovarian carcinoma. Cancer Lett. 432:144–155. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang F, Parayath NN, Ene CI, Stephan SB, Koehne AL, Coon ME, Holland EC and Stephan MT: Genetic programming of macrophages to perform anti-tumor functions using targeted mRNA nanocarriers. Nat Commun. 10:39742019. View Article : Google Scholar : PubMed/NCBI | |
|
Chen D, Xie J, Fiskesund R, Dong W, Liang X, Lv J, Jin X, Liu J, Mo S, Zhang T, et al: Chloroquine modulates antitumor immune response by resetting tumor-associated macrophages toward M1 phenotype. Nat Commun. 9:8732018. View Article : Google Scholar : PubMed/NCBI | |
|
Bellora F, Castriconi R, Dondero A, Pessino A, Nencioni A, Liggieri G, Moretta L, Mantovani A, Moretta A and Bottino C: TLR activation of tumor-associated macrophages from ovarian cancer patients triggers cytolytic activity of NK cells. Eur J Immunol. 44:1814–1822. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ma L, Zhu M, Gai J, Li G, Chang Q, Qiao P, Cao L, Chen W, Zhang S and Wan Y: Preclinical development of a novel CD47 nanobody with less toxicity and enhanced anti-cancer therapeutic potential. J Nanobiotechnology. 18:122020. View Article : Google Scholar : PubMed/NCBI | |
|
Rakina M, Kazakova A, Villert A, Kolomiets L and Larionova I: Spheroid formation and peritoneal metastasis in ovarian cancer: The role of stromal and immune components. Int J Mol Sci. 23:62152022. View Article : Google Scholar : PubMed/NCBI | |
|
Long L, Yin M and Min W: 3D co-culture system of tumor-associated macrophages and ovarian cancer cells. Bio Protoc. 8:e28152018.PubMed/NCBI |
