Role of the tumor microenvironment in the lymphatic metastasis of cervical cancer (Review)
- Authors:
- Lufang Wang
- Shuyan Yi
- Yun Teng
- Wenhan Li
- Jing Cai
-
Affiliations: Department of Obstetrics and Gynecology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China, Department of Laboratory Medicine, The First Affiliated Hospital, Zhejiang University School of Medicine; Key Laboratory of Clinical In Vitro Diagnostic Techniques of Zhejiang Province; Institute of Laboratory Medicine, Zhejiang University, Hangzhou, Zhejiang 310000, P.R. China, Department of Obstetrics and Gynecology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China - Published online on: September 1, 2023 https://doi.org/10.3892/etm.2023.12185
- Article Number: 486
-
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Singh D, Vignat J, Lorenzoni V, Eslahi M, Ginsburg O, Lauby-Secretan B, Arbyn M, Basu P, Bray F and Vaccarella S: Global estimates of incidence and mortality of cervical cancer in 2020: A baseline analysis of the WHO global cervical cancer elimination initiative. Lancet Glob Health. 11:e197–e206. 2023.PubMed/NCBI View Article : Google Scholar | |
Tax C, Rovers MM, de Graaf C, Zusterzeel PL and Bekkers RL: The sentinel node procedure in early stage cervical cancer, taking the next step; a diagnostic review. Gynecol Oncol. 139:559–567. 2015.PubMed/NCBI View Article : Google Scholar | |
Bhatla N, Aoki D, Sharma DN and Sankaranarayanan R: Cancer of the cervix uteri. Int J Gynaecol Obstet. 143 (Suppl 2):S22–S36. 2018.PubMed/NCBI View Article : Google Scholar | |
Jürgenliemk-Schulz IM, Beriwal S, de Leeuw AAC, Lindegaard JC, Nomden CN, Pötter R, Tanderup K, Viswanathan AN and Erickson B: Management of nodal disease in advanced cervical cancer. Semin Radiat Oncol. 29:158–165. 2019.PubMed/NCBI View Article : Google Scholar | |
Dadafarin S, Carnazza M, Islam HK, Moscatello A, Tiwari RK and Geliebter J: Noncoding RNAs in papillary thyroid cancer: Interaction with cancer-associated fibroblasts (CAFs) in the tumor microenvironment (TME) and regulators of differentiation and lymph node metastasis. Adv Exp Med Biol. 1350:145–155. 2021.PubMed/NCBI View Article : Google Scholar | |
Solis-Castillo LA, Garcia-Romo GS, Diaz-Rodriguez A, Reyes-Hernandez D, Tellez-Rivera E, Rosales-Garcia VH, Mendez-Cruz AR, Jimenez-Flores JR, Villafana-Vazquez VH and Pedroza-Gonzalez A: Tumor-infiltrating regulatory T cells, CD8/Treg ratio, and cancer stem cells are correlated with lymph node metastasis in patients with early breast cancer. Breast Cancer. 27:837–849. 2020.PubMed/NCBI View Article : Google Scholar | |
Griffith JW, Sokol CL and Luster AD: Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu Rev Immunol. 32:659–702. 2014.PubMed/NCBI View Article : Google Scholar | |
Singh S, Sadanandam A and Singh RK: Chemokines in tumor angiogenesis and metastasis. Cancer Metastasis Rev. 26:453–467. 2007.PubMed/NCBI View Article : Google Scholar | |
He M, He Q, Cai X, Chen Z, Lao S, Deng H, Liu X, Zheng Y, Liu X, Liu J, et al: Role of lymphatic endothelial cells in the tumor microenvironment-a narrative review of recent advances. Transl Lung Cancer Res. 10:2252–2277. 2021.PubMed/NCBI View Article : Google Scholar | |
Schito L: Hypoxia-dependent angiogenesis and lymphangiogenesis in cancer. Adv Exp Med Biol. 1136:71–85. 2019.PubMed/NCBI View Article : Google Scholar | |
Ji RC: Hypoxia and lymphangiogenesis in tumor microenvironment and metastasis. Cancer Lett. 346:6–16. 2014.PubMed/NCBI View Article : Google Scholar | |
Dieterich LC, Tacconi C, Ducoli L and Detmar M: Lymphatic vessels in cancer. Physiol Rev. 102:1837–1879. 2022.PubMed/NCBI View Article : Google Scholar | |
Chen JM, Luo B, Ma R, Luo XX, Chen YS and Li Y: Lymphatic endothelial markers and tumor lymphangiogenesis assessment in human breast cancer. Diagnostics (Basel). 12(4)2021.PubMed/NCBI View Article : Google Scholar | |
Lambert AW and Weinberg RA: Linking EMT programmes to normal and neoplastic epithelial stem cells. Nat Rev Cancer. 21:325–338. 2021.PubMed/NCBI View Article : Google Scholar | |
Bakir B, Chiarella AM, Pitarresi JR and Rustgi AK: EMT, MET, plasticity, and tumor metastasis. Trends Cell Biol. 30:764–776. 2020.PubMed/NCBI View Article : Google Scholar | |
Sinha D, Saha P, Samanta A and Bishayee A: Emerging concepts of hybrid epithelial-to-mesenchymal transition in cancer progression. Biomolecules. 10(1561)2020.PubMed/NCBI View Article : Google Scholar | |
Kumagai Y, Tachikawa T, Higashi M, Sobajima J, Takahashi A, Amano K, Fukuchi M, Ishibashi K, Mochiki E, Yakabi K, et al: Vascular endothelial growth factors C and D and lymphangiogenesis at the early stage of esophageal squamous cell carcinoma progression. Dis Esophagus. 31:2018.PubMed/NCBI View Article : Google Scholar | |
García-Silva S, Benito-Martín A, Nogués L, Hernández-Barranco A, Mazariegos MS, Santos V, Hergueta-Redondo M, Ximénez-Embún P, Kataru RP, Lopez AA, et al: Melanoma-derived small extracellular vesicles induce lymphangiogenesis and metastasis through an NGFR-dependent mechanism. Nat Cancer. 2:1387–1405. 2021.PubMed/NCBI View Article : Google Scholar | |
Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S, Mihm MC and Detmar M: Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol. 18:1232–1242. 2005.PubMed/NCBI View Article : Google Scholar | |
Roy S, Kumaravel S, Banerjee P, White TK, O'Brien A, Seelig C, Chauhan R, Ekser B, Bayless KJ, Alpini G, et al: Tumor lymphatic interactions induce CXCR2-CXCL5 axis and alter cellular metabolism and lymphangiogenic pathways to promote cholangiocarcinoma. Cells. 10(3093)2021.PubMed/NCBI View Article : Google Scholar | |
Gogineni A, Maresa C, Ailey C, Lee CR, Fuh G, van Bruggen N, Ye W and Weimer RM: Inhibition of VEGF-C modulates distal lymphatic remodeling and secondary metastasis. PLoS One. 8(e68755)2013.PubMed/NCBI View Article : Google Scholar | |
Aebischer D, Iolyeva M and Halin C: The inflammatory response of lymphatic endothelium. Angiogenesis. 17:383–393. 2014.PubMed/NCBI View Article : Google Scholar | |
Miteva DO, Rutkowski JM, Dixon JB, Kilarski W, Shields JD and Swartz MA: Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res. 106:920–931. 2010.PubMed/NCBI View Article : Google Scholar | |
Wiley HE, Gonzalez EB, Maki W, Wu MT and Wang ST: Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Nat Cancer Inst. 93:1638–1643. 2001.PubMed/NCBI View Article : Google Scholar | |
Mezzapelle R, Leo M, Caprioglio F, Colley LS, Lamarca A, Sabatino L, Colantuoni V, Crippa MP and Bianchi ME: CXCR4/CXCL12 activities in the tumor microenvironment and implications for tumor immunotherapy. Cancers (Basel). 14(2314)2022.PubMed/NCBI View Article : Google Scholar | |
Hirakawa S, Detmar M, Kerjaschki D, Nagamatsu S, Matsuo K, Tanemura A, Kamata N, Higashikawa K, Okazaki H, Kameda K, et al: Nodal lymphangiogenesis and metastasis: Role of tumor-induced lymphatic vessel activation in extramammary Paget's disease. Am J Pathol. 175:2235–2248. 2009.PubMed/NCBI View Article : Google Scholar | |
Kawada K, Hosogi H, Sonoshita M, Sakashita H, Manabe T, Shimahara Y, Sakai Y, Takabayashi A, Oshima M and Taketo MM: Chemokine receptor CXCR3 promotes colon cancer metastasis to lymph nodes. Oncogene. 26:4679–4688. 2007.PubMed/NCBI View Article : Google Scholar | |
Das S, Sarrou E, Podgrabinska S, Cassella M, Mungamuri SK, Feirt N, Gordon R, Nagi CS, Wang Y, Entenberg D, et al: Tumor cell entry into the lymph node is controlled by CCL1 chemokine expressed by lymph node lymphatic sinuses. J Exp Med. 210:1509–1528. 2013.PubMed/NCBI View Article : Google Scholar | |
Fujimoto N and Dieterich LC: Mechanisms and clinical significance of tumor lymphatic invasion. Cells. 10(2585)2021.PubMed/NCBI View Article : Google Scholar | |
Issa A, Le TX, Shoushtari AN, Shields JD and Swartz MA: Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-talk promote invasive phenotype. Cancer Res. 69:349–357. 2009.PubMed/NCBI View Article : Google Scholar | |
Meier F, Will S, Ellwanger U, Schlagenhauff B, Schittek B, Rassner G and Garbe C: Metastatic pathways and time courses in the orderly progression of cutaneous melanoma. Br J Dermatol. 147:62–70. 2002.PubMed/NCBI View Article : Google Scholar | |
Kim M, Koh YJ, Kim KE, Koh BI, Nam DH, Alitalo K, Kim I and Koh GY: CXCR4 signaling regulates metastasis of chemoresistant melanoma cells by a lymphatic metastatic niche. Cancer Res. 70:10411–10421. 2010.PubMed/NCBI View Article : Google Scholar | |
Farnsworth RH, Karnezis T, Maciburko SJ, Mueller SN and Stacker SA: The interplay between lymphatic vessels and chemokines. Front Immunol. 10(518)2019.PubMed/NCBI View Article : Google Scholar | |
Shields JD, Kourtis IC, Tomei AA, Roberts JM and Swartz MA: Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science. 328:749–752. 2010.PubMed/NCBI View Article : Google Scholar | |
Lund AW, Duraes FV, Hirosue S, Raghavan VR, Nembrini C, Thomas S, Issa A, Hugues S and Swartz MA: VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigen by lymph node lymphatics. Cell Rep. 1:191–199. 2012.PubMed/NCBI View Article : Google Scholar | |
Tewalt EF, Cohen JN, Rouhani SJ, Guidi CJ, Qiao H, Fahl SP, Conaway MR, Bender TP, Tung KS, Vella AT, et al: Lymphatic endothelial cells induce tolerance via PD-L1 and lack of costimulation leading to high-level PD-1 expression on CD8 T cells. Blood. 120:4772–4782. 2012.PubMed/NCBI View Article : Google Scholar | |
De Nola R, Loizzi V, Cicinelli E and Cormio G: Dynamic crosstalk within the tumor microenvironment of uterine cervical carcinoma: Baseline network, iatrogenic alterations, and translational implications. Crit Rev Oncol Hematol. 162(103343)2021.PubMed/NCBI View Article : Google Scholar | |
Datta A, West C, O'Connor JPB, Choudhury A and Hoskin P: Impact of hypoxia on cervical cancer outcomes. Int J Gynecol Cancer. 31:1459–1470. 2021.PubMed/NCBI View Article : Google Scholar | |
Rojo-León V, García C, Valencia C, Méndez MA, Wood C and Covarrubias L: The E6/E7 oncogenes of human papilloma virus and estradiol regulate hedgehog signaling activity in a murine model of cervical cancer. Exp Cell Res. 381:311–322. 2019.PubMed/NCBI View Article : Google Scholar | |
De Nola R, Menga A, Castegna A, Loizzi V, Ranieri G, Cicinelli E and Cormio G: The crowded crosstalk between cancer cells and stromal microenvironment in gynecological malignancies: Biological pathways and therapeutic implication. Int J Mol Sci. 20(2401)2019.PubMed/NCBI View Article : Google Scholar | |
Lea JS and Lin KY: Cervical cancer. Obstet Gynecol Clin North Am. 39:233–253. 2012.PubMed/NCBI View Article : Google Scholar | |
Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E and McDonald DM: Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med. 204:2349–2362. 2007.PubMed/NCBI View Article : Google Scholar | |
Tacconi C, Correale C, Gandelli A, Spinelli A, Dejana E, D'Alessio S and Danese S: Vascular endothelial growth factor C disrupts the endothelial lymphatic barrier to promote colorectal cancer invasion. Gastroenterology. 148:1438–1451.e8. 2015.PubMed/NCBI View Article : Google Scholar | |
Chen C, Shen N, Chen Y, Jiang P, Sun W, Wang Q, Wang Z, Wang Y, Cheng W, Fu S and Wang S: LncCCLM inhibits lymphatic metastasis of cervical cancer by promoting STAU1-mediated IGF-1 mRNA degradation. Cancer Lett. 518:169–179. 2021.PubMed/NCBI View Article : Google Scholar | |
Alavi A, Carlin SD, Werner TJ and Zaghal AA: Suboptimal sensitivity and specificity of PET and other gross imaging techniques in assessing lymph node metastasis. Mol Imaging Biol. 21:808–811. 2019.PubMed/NCBI View Article : Google Scholar | |
Phan TG and Croucher PI: The dormant cancer cell life cycle. Nat Rev Cancer. 20:398–411. 2020.PubMed/NCBI View Article : Google Scholar | |
Ju S, Wang F, Wang Y and Ju S: CSN8 is a key regulator in hypoxia-induced epithelial-mesenchymal transition and dormancy of colorectal cancer cells. Mol Cancer. 19(168)2020.PubMed/NCBI View Article : Google Scholar | |
Hsin MC, Hsieh YH, Hsiao YH, Chen PN, Wang PH and Yang SF: Carbonic anhydrase IX promotes human cervical cancer cell motility by regulating PFKFB4 expression. Cancers (Basel). 13(1174)2021.PubMed/NCBI View Article : Google Scholar | |
Sugiura K, Nakajima S, Kato I, Okubo-Sato M, Nakazawa Y, Mitsudo K and Kioi M: Hypoxia and CD11b+ cell influx are strongly associated with lymph node metastasis of oral cancer. Anticancer Res. 40:6845–6852. 2020.PubMed/NCBI View Article : Google Scholar | |
Cairns RA and Hill RP: Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma. Cancer Res. 64:2054–2061. 2004.PubMed/NCBI View Article : Google Scholar | |
Chaudary N, Milosevic M and Hill RP: Suppression of vascular endothelial growth factor receptor 3 (VEGFR3) and vascular endothelial growth factor C (VEGFC) inhibits hypoxia-induced lymph node metastases in cervix cancer. Gynecol Oncol. 123:393–400. 2011.PubMed/NCBI View Article : Google Scholar | |
Lee S, Shin HJ, Han IO, Hong EK, Park SY, Roh JW, Shin KH, Kim TH and Kim JY: Tumor carbonic anhydrase 9 expression is associated with the presence of lymph node metastases in uterine cervical cancer. Cancer Sci. 98:329–333. 2007.PubMed/NCBI View Article : Google Scholar | |
Li Z, Jiang L, Chew SH, Hirayama T, Sekido Y and Toyokuni S: Carbonic anhydrase 9 confers resistance to ferroptosis/apoptosis in malignant mesothelioma under hypoxia. Redox Biol. 26(101297)2019.PubMed/NCBI View Article : Google Scholar | |
Hu HM, Mao MH, Hu YH, Zhou XC, Li S, Chen CF, Li CN, Yuan QL and Li W: Artemisinin protects DPSC from hypoxia and TNF-α mediated osteogenesis impairments through CA9 and Wnt signaling pathway. Life Sci. 277(119471)2021.PubMed/NCBI View Article : Google Scholar | |
Kim JH, Kim JY, Yoon MS, Kim YS, Lee JH, Kim HJ, Kim H, Kim YJ, Yoo CW, Nam BH, et al: Prophylactic irradiation of para-aortic lymph nodes for patients with locally advanced cervical cancers with and without high CA9 expression (KROG 07-01): A randomized, open-label, multicenter, phase 2 trial. Radiother Oncol. 120:383–389. 2016.PubMed/NCBI View Article : Google Scholar | |
Chen XJ, Deng YR, Wang ZC, Wei WF, Zhou CF, Zhang YM, Yan RM, Liang LJ, Zhong M, Liang L, et al: Hypoxia-induced ZEB1 promotes cervical cancer progression via CCL8-dependent tumour-associated macrophage recruitment. Cell Death Dis. 10(508)2019.PubMed/NCBI View Article : Google Scholar | |
Chen XJ, Wei WF, Wang ZC, Wang N, Guo CH, Zhou CF, Liang LJ, Wu S, Liang L and Wang W: A novel lymphatic pattern promotes metastasis of cervical cancer in a hypoxic tumour-associated macrophage-dependent manner. Angiogenesis. 24:549–565. 2021.PubMed/NCBI View Article : Google Scholar | |
Chen XJ, Wu S, Yan RM, Fan LS, Yu L, Zhang YM, Wei WF, Zhou CF, Wu XG, Zhong M, et al: The role of the hypoxia-Nrp-1 axis in the activation of M2-like tumor-associated macrophages in the tumor microenvironment of cervical cancer. Mol Carcinog. 58:388–397. 2019.PubMed/NCBI View Article : Google Scholar | |
Mao X, Xu J, Wang W, Liang C, Hua J, Liu J, Zhang B, Meng Q, Yu X and Shi S: Crosstalk between cancer-associated fibroblasts and immune cells in the tumor microenvironment: New findings and future perspectives. Mol Cance. 20(131)2021.PubMed/NCBI View Article : Google Scholar | |
Huang M, Fu M, Wang J, Xia C, Zhang H, Xiong Y, He J, Liu J, Liu B, Pan S and Liu F: TGF-β1-activated cancer-associated fibroblasts promote breast cancer invasion, metastasis and epithelial-mesenchymal transition by autophagy or overexpression of FAP-α. Biochem Pharmacol. 188(114527)2021.PubMed/NCBI View Article : Google Scholar | |
Wang Y, Jing Y, Ding L, Zhang X, Song Y, Chen S, Zhao X, Huang X, Pu Y, Wang Z, et al: Epiregulin reprograms cancer-associated fibroblasts and facilitates oral squamous cell carcinoma invasion via JAK2-STAT3 pathway. J Exp Clin Cancer Res. 38(274)2019.PubMed/NCBI View Article : Google Scholar | |
Zhou B, Chen WL, Wang YY, Lin ZY, Zhang DM, Fan S and Li JS: A role for cancer-associated fibroblasts in inducing the epithelial-to-mesenchymal transition in human tongue squamous cell carcinoma. J Oral Pathol Med. 43:585–592. 2014.PubMed/NCBI View Article : Google Scholar | |
Murata T, Mekada E and Hoffman RM: Reconstitution of a metastatic-resistant tumor microenvironment with cancer-associated fibroblasts enables metastasis. Cell Cycle. 16:533–535. 2017.PubMed/NCBI View Article : Google Scholar | |
Murata T, Mizushima H, Chinen I, Moribe H, Yagi S, Hoffman RM, Kimura T, Yoshino K, Ueda Y, Enomoto T and Mekada E: HB-EGF and PDGF mediate reciprocal interactions of carcinoma cells with cancer-associated fibroblasts to support progression of uterine cervical cancers. Cancer Res. 71:6633–6642. 2011.PubMed/NCBI View Article : Google Scholar | |
Xiao L, Zhu H, Shu J, Gong D, Zheng D and Gao J: Overexpression of TGF-β1 and SDF-1 in cervical cancer-associated fibroblasts promotes cell growth, invasion and migration. Arch Gynecol Obstet. 305:179–192. 2022.PubMed/NCBI View Article : Google Scholar | |
Wei WF, Chen XJ, Liang LJ, Yu L, Wu XG, Zhou CF, Wang ZC, Fan LS, Hu Z, Liang L and Wang W: Periostin+ cancer-associated fibroblasts promote lymph node metastasis by impairing the lymphatic endothelial barriers in cervical squamous cell carcinoma. Mol Oncol. 15:210–227. 2021.PubMed/NCBI View Article : Google Scholar | |
Nielsen SR and Schmid MC: Macrophages as key drivers of cancer progression and metastasis. Mediators Inflamm. 2017(9624760)2017.PubMed/NCBI View Article : Google Scholar | |
Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, Politi LS, Gentner B, Brown JL, Naldini L and De Palma M: Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell. 19:512–526. 2011.PubMed/NCBI View Article : Google Scholar | |
Yeo EJ, Cassetta L, Qian BZ, Lewkowich I, Li JF, Stefater JA III, Smith AN, Wiechmann LS, Wang Y, Pollard JW and Lang RA: Myeloid WNT7b mediates the angiogenic switch and metastasis in breast cancer. Cancer Res. 74:2962–2973. 2014.PubMed/NCBI View Article : Google Scholar | |
Ji H, Cao R, Yang Y, Zhang Y, Iwamoto H, Lim S, Nakamura M, Andersson P, Wang J, Sun Y, et al: TNFR1 mediates TNF-α-induced tumour lymphangiogenesis and metastasis by modulating VEGF-C-VEGFR3 signalling. Nat Commun. 5(4944)2014.PubMed/NCBI View Article : Google Scholar | |
Kimura S, Noguchi H, Nanbu U and Nakayama T: Macrophage CCL22 expression promotes lymphangiogenesis in patients with tongue squamous cell carcinoma via IL-4/STAT6 in the tumor microenvironment. Oncol Lett. 21(383)2021.PubMed/NCBI View Article : Google Scholar | |
Hosono M, Koma YI, Takase N, Urakawa N, Higashino N, Suemune K, Kodaira H, Nishio M, Shigeoka M, Kakeji Y and Yokozaki H: CXCL8 derived from tumor-associated macrophages and esophageal squamous cell carcinomas contributes to tumor progression by promoting migration and invasion of cancer cells. Oncotarget. 8:106071–106088. 2017.PubMed/NCBI View Article : Google Scholar | |
Guo F, Kong W, Zhao G, Cheng Z, Ai L, Lv J, Feng Y and Ma X: The correlation between tumor-associated macrophage infiltration and progression in cervical carcinoma. Biosci Rep. 41(BSR20203145)2021.PubMed/NCBI View Article : Google Scholar | |
Tan J, Yang L, Zhao H, Ai Y, Ren L, Zhang F, Dong W, Shi R, Sun D and Feng Y: The role of NFATc1/c-myc/PKM2/IL-10 axis in activating cervical cancer tumor-associated M2 macrophage polarization to promote cervical cancer progression. Exp Cell Res. 413(113052)2022.PubMed/NCBI View Article : Google Scholar | |
Jiang S, Yang Y, Fang M, Li X and Yuan XJ: Co-evolution of tumor-associated macrophages and tumor neo-vessels during cervical cancer invasion. Oncol Lett. 12:2625–2631. 2016.PubMed/NCBI View Article : Google Scholar | |
Li Y, Huang G and Zhang S: Associations between intratumoral and peritumoral M2 macrophage counts and cervical squamous cell carcinoma invasion patterns. Int J Gynaecol Obstet. 139:346–351. 2017.PubMed/NCBI View Article : Google Scholar | |
Dou A and Fang J: Heterogeneous myeloid cells in tumors. Cancers (Basel). 13(3772)2021.PubMed/NCBI View Article : Google Scholar | |
Mabuchi S, Matsumoto Y, Kawano M, Minami K, Seo Y, Sasano T, Takahashi R, Kuroda H, Hisamatsu T, Kakigano A, et al: Uterine cervical cancer displaying tumor-related leukocytosis: A distinct clinical entity with radioresistant feature. J Natl Cancer Inst. 106(dju147)2014.PubMed/NCBI View Article : Google Scholar | |
Marvel D and Gabrilovich DI: Myeloid-derived suppressor cells in the tumor microenvironment: Expect the unexpected. J Clin Invest. 125:3356–3364. 2015.PubMed/NCBI View Article : Google Scholar | |
Mabuchi S, Komura N, Sasano T, Shimura K, Yokoi E, Kozasa K, Kuroda H, Takahashi R, Kawano M, Matsumoto Y, et al: Pretreatment tumor-related leukocytosis misleads positron emission tomography-computed tomography during lymph node staging in gynecological malignancies. Nat Commun. 11(1364)2020.PubMed/NCBI View Article : Google Scholar | |
Lee BR, Kwon BE, Hong EH, Shim A, Song JH, Kim HM, Chang SY, Kim YJ, Kweon MN, Youn JI and Ko HJ: Interleukin-10 attenuates tumour growth by inhibiting interleukin-6/signal transducer and activator of transcription 3 signalling in myeloid-derived suppressor cells. Cancer Lett. 381:156–164. 2016.PubMed/NCBI View Article : Google Scholar | |
Kim KH, Sim NS, Chang JS and Kim YB: Tumor immune microenvironment in cancer patients with leukocytosis. Cancer Immunol Immunother. 69:1265–1277. 2020.PubMed/NCBI View Article : Google Scholar | |
Panni RZ, Sanford DE, Belt BA, Mitchem JB, Worley LA, Goetz BD, Mukherjee P, Wang-Gillam A, Link DC, Denardo DG, et al: Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol Immunother. 63:513–528. 2014.PubMed/NCBI View Article : Google Scholar | |
Peng D, Tanikawa T, Li W, Zhao L, Vatan L, Szeliga W, Wan S, Wei S, Wang Y, Liu Y, et al: Myeloid-derived suppressor cells endow stem-like qualities to breast cancer cells through IL6/STAT3 and NO/NOTCH cross-talk signaling. Cancer Res. 76:3156–3165. 2016.PubMed/NCBI View Article : Google Scholar | |
Kuroda H, Mabuchi S, Yokoi E, Komura N, Kozasa K, Matsumoto Y, Kawano M, Takahashi R, Sasano T, Shimura K, et al: Prostaglandin E2 produced by myeloid-derived suppressive cells induces cancer stem cells in uterine cervical cancer. Oncotarget. 9:36317–36330. 2018.PubMed/NCBI View Article : Google Scholar | |
Ni HH, Zhang L, Huang H, Dai SQ and Li J: Connecting METTL3 and intratumoural CD33+ MDSCs in predicting clinical outcome in cervical cancer. J Transl Med. 18(393)2020.PubMed/NCBI View Article : Google Scholar | |
Heeren AM, Koster BD, Samuels S, Ferns DM, Chondronasiou D, Kenter GG, Jordanova ES and de Gruijl TD: High and interrelated rates of PD-L1+CD14+ antigen-presenting cells and regulatory T cells mark the microenvironment of metastatic lymph nodes from patients with cervical cancer. Cancer Immunol Res. 3:48–58. 2015.PubMed/NCBI View Article : Google Scholar | |
Rodríguez PC and Ochoa AC: Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: Mechanisms and therapeutic perspectives. Immunol Rev. 222:180–191. 2008.PubMed/NCBI View Article : Google Scholar | |
Galliverti G, Wullschleger S, Tichet M, Murugan D, Zangger N, Horton W, Korman AJ, Coussens LM, Swartz MA and Hanahan D: Myeloid cells orchestrate systemic immunosuppression, impairing the efficacy of immunotherapy against HPV+ cancers. Cancer Immunol Res. 8:131–145. 2020.PubMed/NCBI View Article : Google Scholar | |
Jianyi D, Haili G, Bo Y, Meiqin Y, Baoyou H, Haoran H, Fang L, Qingliang Z and Lingfei H: Myeloid-derived suppressor cells cross-talk with B10 cells by BAFF/BAFF-R pathway to promote immunosuppression in cervical cancer. Cancer Immunol Immunother. 72:87–89. 2023.PubMed/NCBI View Article : Google Scholar | |
Kawano M, Mabuchi S, Matsumoto Y, Sasano T, Takahashi R, Kuroda H, Kozasa K, Hashimoto K, Isobe A, Sawada K, et al: The significance of G-CSF expression and myeloid-derived suppressor cells in the chemoresistance of uterine cervical cancer. Sci Rep. 5(18217)2015.PubMed/NCBI View Article : Google Scholar | |
Sawant DV, Yano H, Chikina M, Zhang Q, Liao M, Liu C, Callahan DJ, Sun Z, Sun T, Tabib T, et al: Adaptive plasticity of IL-10+ and IL-35+ Treg cells cooperatively promotes tumor T cell exhaustion. Nat Immunol. 20:724–735. 2019.PubMed/NCBI View Article : Google Scholar | |
Wu MY, Kuo TY and Ho HN: Tumor-infiltrating lymphocytes contain a higher proportion of FOXP3(+) T lymphocytes in cervical cancer. J Formos Med Assoc. 110:580–586. 2011.PubMed/NCBI View Article : Google Scholar | |
Nakamura T, Shima T, Saeki A, Hidaka T, Nakashima A, Takikawa O and Saito S: Expression of indoleamine 2, 3-dioxygenase and the recruitment of Foxp3-expressing regulatory T cells in the development and progression of uterine cervical cancer. Cancer Sci. 98:874–881. 2007.PubMed/NCBI View Article : Google Scholar | |
Heeren AM, de Boer E, Bleeker MC, Musters RJ, Buist MR, Kenter GG, de Gruijl TD and Jordanova ES: Nodal metastasis in cervical cancer occurs in clearly delineated fields of immune suppression in the pelvic lymph catchment area. Oncotarget. 6:32484–32493. 2015.PubMed/NCBI View Article : Google Scholar | |
Wang S, Li J, Xie J, Liu F, Duan Y, Wu Y, Huang S, He X, Wang Z and Wu X: Programmed death ligand 1 promotes lymph node metastasis and glucose metabolism in cervical cancer by activating integrin β4/SNAI1/SIRT3 signaling pathway. Oncogene. 37:4164–4180. 2018.PubMed/NCBI View Article : Google Scholar | |
Stein M and Eckert KA: Impact of G-quadruplexes and chronic inflammation on genome instability: Additive effects during carcinogenesis. Genes (Basel). 12(1779)2021.PubMed/NCBI View Article : Google Scholar | |
Zhang LX, Wei ZJ, Xu M and Zang JH: Can the neutrophil-lymphocyte ratio and platelet-lymphocyte ratio be beneficial in predicting lymph node metastasis and promising prognostic markers of gastric cancer patients? Tumor maker retrospective study. Int J Surg. 56:320–327. 2018.PubMed/NCBI View Article : Google Scholar | |
Ayhan S, Akar S, Kar İ, Turan AT, Türkmen O, Kiliç F, Aytekin O, Ersak B, Ceylan Ö, Moraloğlu Tekin Ö and Kimyon Comert G: Prognostic value of systemic inflammatory response markers in cervical cancer. J Obstet Gynaecol. 42(2411)2022.PubMed/NCBI View Article : Google Scholar | |
Lee WH, Kim GE and Kim YB: Prognostic factors of dose-response relationship for nodal control in metastatic lymph nodes of cervical cancer patients undergoing definitive radiotherapy with concurrent chemotherapy. J Gynecol Oncol. 33(e59)2022.PubMed/NCBI View Article : Google Scholar | |
Polgár C, Major T and Varga S: Radiotherapy and radio-chemotherapy of cervical cancer. Magy Onkol. 66:307–314. 2022.PubMed/NCBI(In Hungarian). | |
Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J, Elkord E, Lichtor T, Decker WK, Whelan RL, Kumara HMCS, et al: Immune evasion in cancer: Mechanistic basis and therapeutic strategies. Semin Cancer Biol. 35 (Suppl):S185–S198. 2015.PubMed/NCBI View Article : Google Scholar | |
van Weelden WJ, Sekarutami SM, Bekkers RL, Kaanders JH, Bussink J, Gondhowiardjo S, Leer JW and Span PN: The effect of carbogen breathing and nicotinamide added to standard (chemo) radiation treatment of advanced cervical cancer in Indonesia. Int J Gynecol Cancer. 24:1628–1635. 2014.PubMed/NCBI View Article : Google Scholar | |
Samsuri NAB, Leech M and Marignol L: Metformin and improved treatment outcomes in radiation therapy-A review. Cancer Treat Rev. 55:150–162. 2017.PubMed/NCBI View Article : Google Scholar | |
Lin A and Maity A: Molecular pathways: A novel approach to targeting hypoxia and improving radiotherapy efficacy via reduction in oxygen demand. Clin Cancer Res. 21:1995–2000. 2015.PubMed/NCBI View Article : Google Scholar | |
Sharma A, Arambula JF, Koo S, Kumar R, Singh H, Sessler JL and Kim JS: Hypoxia-targeted drug delivery. Chem Soc Rev. 48:771–813. 2019.PubMed/NCBI View Article : Google Scholar | |
Zeman EM, Brown JM, Lemmon MJ, Hirst VK and Lee WW: SR-4233: A new bioreductive agent with high selective toxicity for hypoxic mammalian cells. Int J Radiat Oncol Biol Phys. 12:1239–1242. 1986.PubMed/NCBI View Article : Google Scholar | |
Brown JM: SR 4233 (tirapazamine): A new anticancer drug exploiting hypoxia in solid tumours. Br J Cancer. 67:1163–1170. 1993.PubMed/NCBI View Article : Google Scholar | |
DiSilvestro PA, Ali S, Craighead PS, Lucci JA, Lee YC, Cohn DE, Spirtos NM, Tewari KS, Muller C, Gajewski WH, et al: Phase III randomized trial of weekly cisplatin and irradiation versus cisplatin and tirapazamine and irradiation in stages IB2, IIA, IIB, IIIB, and IVA cervical carcinoma limited to the pelvis: A gynecologic oncology group study. J Clin Oncol. 32:458–464. 2014.PubMed/NCBI View Article : Google Scholar | |
Seidel JA, Otsuka A and Kabashima K: Anti-PD-1 and anti-CTLA-4 therapies in cancer: Mechanisms of action, efficacy, and limitations. Front Oncol. 8(86)2018.PubMed/NCBI View Article : Google Scholar | |
Chen DS and Mellman I: Oncology meets immunology: The cancer-immunity cycle. Immunity. 39:1–10. 2013.PubMed/NCBI View Article : Google Scholar | |
Yao S, Zhu Y and Chen L: Advances in targeting cell surface signalling molecules for immune modulation. Nat Rev Drug Discov. 12:130–146. 2013.PubMed/NCBI View Article : Google Scholar | |
Naumann RW, Hollebecque A, Meyer T, Devlin MJ, Oaknin A, Kerger J, López-Picazo JM, Machiels JP, Delord JP, Evans TRJ, et al: Safety and efficacy of Nivolumab Monotherapy in recurrent or metastatic cervical, vaginal, or vulvar carcinoma: Results from the phase I/II CheckMate 358 trial. J Clin Oncol. 37:2825–2834. 2019.PubMed/NCBI View Article : Google Scholar | |
O'Malley DM, Neffa M, Monk BJ, Melkadze T, Huang M, Kryzhanivska A, Bulat I, Meniawy TM, Bagameri A, Wang EW, et al: Dual PD-1 and CTLA-4 checkpoint blockade using Balstilimab and Zalifrelimab combination as second-line treatment for advanced cervical cancer: An open-label phase II study. J Clin Oncol. 40:762–771. 2022.PubMed/NCBI View Article : Google Scholar | |
Santin AD, Deng W, Frumovitz M, Buza N, Bellone S, Huh W, Khleif S, Lankes HA, Ratner ES, O'Cearbhaill RE, et al: Phase II evaluation of nivolumab in the treatment of persistent or recurrent cervical cancer (NCT02257528/NRG-GY002). Gynecol Oncol. 157:161–166. 2020.PubMed/NCBI View Article : Google Scholar | |
Frenel JS, Le Tourneau C, O'Neil B, Ott PA, Piha-Paul SA, Gomez-Roca C, van Brummelen EMJ, Rugo HS, Thomas S, Saraf S, et al: Safety and efficacy of Pembrolizumab in advanced, programmed death ligand 1-positive cervical cancer: Results from the phase Ib KEYNOTE-028 trial. J Clin Oncol. 35:4035–4041. 2017.PubMed/NCBI View Article : Google Scholar | |
Chung HC, Ros W, Delord JP, Perets R, Italiano A, Shapira-Frommer R, Manzuk L, Piha-Paul SA, Xu L, Zeigenfuss S, et al: Efficacy and safety of pembrolizumab in previously treated advanced cervical cancer: results from the phase II KEYNOTE-158 study. J Clin Oncol. 37:1470–1478. 2019.PubMed/NCBI View Article : Google Scholar | |
De Jaeghere EA, Tuyaerts S, Van Nuffel AMT, Belmans A, Bogaerts K, Baiden-Amissah R, Lippens L, Vuylsteke P, Henry S, Trinh XB, et al: Pembrolizumab, radiotherapy, and an immunomodulatory five-drug cocktail in pretreated patients with persistent, recurrent, or metastatic cervical or endometrial carcinoma: Results of the phase II PRIMMO study. Cancer Immunol Immunother. 72:475–491. 2023.PubMed/NCBI View Article : Google Scholar | |
Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, et al: Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment. Blood. 114:589–595. 2009.PubMed/NCBI View Article : Google Scholar | |
Sharabi AB, Lim M, DeWeese TL and Drake CG: Radiation and checkpoint blockade immunotherapy: Radiosensitisation and potential mechanisms of synergy. Lancet Oncol. 16:e498–e509. 2015.PubMed/NCBI View Article : Google Scholar | |
Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, Benci JL, Xu B, Dada H, Odorizzi PM, et al: Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 520:373–377. 2015.PubMed/NCBI View Article : Google Scholar | |
Young KH, Baird JR, Savage T, Cottam B, Friedman D, Bambina S, Messenheimer DJ, Fox B, Newell P, Bahjat KS, et al: Optimizing timing of immunotherapy improves control of tumors by hypofractionated radiation therapy. PLoS One. 11(e0157164)2016.PubMed/NCBI View Article : Google Scholar | |
Dovedi SJ, Adlard AL, Lipowska-Bhalla G, McKenna C, Jones S, Cheadle EJ, Stratford IJ, Poon E, Morrow M, Stewart R, et al: Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res. 74:5458–5468. 2014.PubMed/NCBI View Article : Google Scholar | |
Sun J and Yuan J: Chemokine (C-X-C motif) ligand 1/chemokine (C-X-C motif) receptor 2 autocrine loop contributes to cellular proliferation, migration and apoptosis in cervical cancer. Bioengineered. 13:7579–7591. 2022.PubMed/NCBI View Article : Google Scholar | |
Strachan DC, Ruffell B, Oei Y, Bissell MJ, Coussens LM, Pryer N and Daniel D: CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8+ T cells. Oncoimmunology. 2(e26968)2013.PubMed/NCBI View Article : Google Scholar | |
Steele CW, Karim SA, Leach JDG, Bailey P, Upstill-Goddard R, Rishi L, Foth M, Bryson S, McDaid K, Wilson Z, et al: CXCR2 inhibition profoundly suppresses metastases and augments immunotherapy in pancreatic ductal adenocarcinoma. Cancer Cell. 29:832–845. 2016.PubMed/NCBI View Article : Google Scholar | |
Pagni RL, Souza PDC, Pegoraro R, Porchia BFMM, da Silva JR, Aps LRMM, Silva MO, Rodrigues KB, Sales NS, Ferreira LCS and Moreno ACR: Interleukin-6 and indoleamine-2,3-dioxygenase as potential adjuvant targets for papillomavirus-related tumors immunotherapy. Front Immunol. 13(1005937)2022.PubMed/NCBI View Article : Google Scholar | |
He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, Takahashi T and Alitalo K: Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst. 94:819–825. 2002.PubMed/NCBI View Article : Google Scholar | |
García-Quiroz J, Vázquez-Almazán B, García-Becerra R, Díaz L and Avila E: The interaction of human papillomavirus infection and prostaglandin E2 signaling in carcinogenesis: A focus on cervical cancer therapeutics. Cells. 11(2528)2022.PubMed/NCBI View Article : Google Scholar | |
Peng H, He X and Wang Q: Immune checkpoint blockades in gynecological cancers: A review of clinical trials. Acta Obstet Gynecol Scand. 101:941–951. 2022.PubMed/NCBI View Article : Google Scholar |