Abstract
High-grade serous ovarian cancer (HGSOC) is the most common and deadly subtype of ovarian cancer as it is commonly diagnosed after substantial metastasis has already occurred. The past two decades have been an active era in HGSOC research, with new information on the origin and genomic signature of the tumor cell. Additionally, studies have begun to characterize changes in the HGSOC microenvironment and examine the impact of these changes on tumor progression and response to therapies. While this knowledge may provide valuable insight into better prognosis and treatments for HGSOCs, its collection, synthesis, and application are complicated by the number of unique microenvironments in the disease—the initiating site (fallopian tube), first metastasis (ovary), distal metastases (peritoneum), and recurrent/platinum-resistant setting. Here, we review the state of our understanding of these diverse sites and highlight remaining questions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
ACS (2016) Cancer facts and figures 2016. American Cancer Society Journal
Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, Bowtell D, Brenton JD (2010) Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol 221(1):49–56. https://doi.org/10.1002/path.2696
Alsina-Sanchis E, Figueras A, Lahiguera A, Vidal A, Casanovas O, Graupera M, Villanueva A, Vinals F (2016) The TGFbeta pathway stimulates ovarian cancer cell proliferation by increasing IGF1R levels. Int J Cancer 139(8):1894–1903. https://doi.org/10.1002/ijc.30233
Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC (2001) Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 22(2):255–288. https://doi.org/10.1210/edrv.22.2.0422
Banet N, Kurman RJ (2015) Two types of ovarian cortical inclusion cysts: proposed origin and possible role in ovarian serous carcinogenesis. Int J Gynecol Pathol 34(1):3–8. https://doi.org/10.1097/PGP.0000000000000120
Bourgeois DL, Kabarowski KA, Porubsky VL, Kreeger PK (2015) High-grade serous ovarian cancer cell lines exhibit heterogeneous responses to growth factor stimulation. Cancer Cell Int 15:112. https://doi.org/10.1186/s12935-015-0263-4
Bregenzer ME, Horst EN, Mehta P, Novak CM, Repetto T, Mehta G (2019) The role of Cancer stem cells and mechanical forces in ovarian Cancer metastasis. Cancers (Basel) 11(7). https://doi.org/10.3390/cancers11071008
Buckley CE, Ren X, Ward LC, Girdler GC, Araya C, Green MJ, Clark BS, Link BA, Clarke JD (2013) Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the zebrafish neural rod. EMBO J 32(1):30–44. https://doi.org/10.1038/emboj.2012.305
Cai J, Tang H, Xu L, Wang X, Yang C, Ruan S, Guo J, Hu S, Wang Z (2012) Fibroblasts in Omentum activated by tumor cells promote ovarian Cancer growth, adhesion, and invasiveness. Carcinogenesis 33(1):20–29
Carroll MJ, Kapur A, Felder M, Patankar MS, Kreeger PK (2016) M2 macrophages induce ovarian cancer cell proliferation via a heparin binding epidermal growth factor/matrix metalloproteinase 9 intercellular feedback loop. Oncotarget 7(52):86608–86620
Carroll MJ, Fogg KC, Patel HA, Krause HB, Mancha AS, Patankar MS, Weisman PS, Barroilhet L, Kreeger PK (2018) Alternatively-activated macrophages upregulate Mesothelial expression of P-selectin to enhance adhesion of ovarian Cancer cells. Cancer Res 78(13):3560–3573. https://doi.org/10.1158/0008-5472.CAN-17-3341
Casey MJ, Synder C, Bewtra C, Narod SA, Watson P, Lynch HT (2005) Intra-abdominal carcinomatosis after prophylactic oophorectomy in women of hereditary breast ovarian cancer syndrome kindreds associated with BRCA1 and BRCA2 mutations. Gynecol Oncol 97(2):457–467. https://doi.org/10.1016/j.ygyno.2005.01.039
Cassetta L, Pollard JW (2018) Targeting macrophages: therapeutic approaches in Cancer. Nat Rev Drug Discov 17(12):887–904
Chegini N, Williams RS (1992) Immunocytochemical localization of transforming growth factors (TGFs) TGF-alpha and TGF-beta in human ovarian tissues. J Clin Endocrinol Metab 74(5):973–980. https://doi.org/10.1210/jcem.74.5.1569174
Chen EY, Mehra K, Mehrad M, Ning G, Miron A, Mutter GL, Monte N, Quade BJ, McKeon FD, Yassin Y, Xian W, Crum CP (2010) Secretory cell outgrowth, PAX2 and serous carcinogenesis in the fallopian tube. J Pathol 222(1):110–116. https://doi.org/10.1002/path.2739
Cheng JC, Auersperg N, Leung PC (2012) EGF-induced EMT and invasiveness in serous borderline ovarian tumor cells: a possible step in the transition to low-grade serous carcinoma cells? PLoS One 7(3):e34071. https://doi.org/10.1371/journal.pone.0034071
Clark R, Krishnan V, Schoof M, Rodriguez I, Theriault B, Chekmareva M, Rinker-Schaeffer C (2013) Milky spots promote ovarian Cancer metastatic colonization of peritoneal adipose in experimental models. Tumorig Neoplastic Progress 183(2):576–591
Corrado G, Salutari V, Palluzzi E, Distefano MG, Scambia G, Ferrandina G (2017) Optimizing treatment in recurrent epithelial ovarian cancer. Expert Rev Anticancer Ther 17(12):1147–1158
Coscia F, Lengyel E, Duraiswamy J, Ashcroft B, Bassani-Sternberg M, Wierer M, Johnson A, Wroblewski K, Montag A, Yamada SD, Lopez-Mendez B, Nilsson J, Mund A, Mann M, Curtis M (2018) Multi-level proteomics identifies CT45 as a Chemosensitivity mediator and immunotherapy target in ovarian Cancer. Cell 175(1):159–170
Curtis M, Kenny HA, Ashcroft B, Mukherjee A, Johnson A, Zhang Y, Helou Y, Batlle R, Liu X, Gutierrez N, Gao X, Yamada SD, Lastra R, Montag A, Ahsan N, Locasale JW, Salomon AR, Nebreda AR, Lengyel E (2019) Fibroblasts mobilize tumor cell glycogen to promote proliferation and metastasis. Cell Metab 29(1):141–155.e149
Dean M, Davis DA, Burdette JE (2017) Activin a stimulates migration of the fallopian tube epithelium, an origin of high-grade serous ovarian cancer, through non-canonical signaling. Cancer Lett 391:114–124
Dean M, Jin V, Russo A, Lantvit DD, Burdette JE (2019) Exposure of the extracellular matrix and colonization of the ovary in metastasis of fallopian-tube-derived cancer. Carcinogenesis 40(1):41–51. https://doi.org/10.1093/carcin/bgy170
Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277(46):43707–43716. https://doi.org/10.1074/jbc.M207105200
Doig T, Monaghan H (2006) Sampling the omentum in ovarian neoplasia: when one block is enough. Int J Gynecol Cancer 16(1):36–40
Ducie J, Dao F, Considine M, Olvera N, Shaw PA, Kurman RJ, Shih IM, Soslow RA, Cope L, Levine DA (2017) Molecular analysis of high-grade serous ovarian carcinoma with and without associated serous tubal intra-epithelial carcinoma. Nat Commun 8(1):990. https://doi.org/10.1038/s41467-017-01217-9
Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, Preisser L, Anegon I, Catala L, Ifrah N, Descamps P, Gamelin E, Gascan H, Hebbar M, Jeannin P (2007) Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 110(13)
Eckert MA, Coscia F, Chryplewicz A, Chang JW, Hernandez KM, Pan S, Tienda SM, Nahotko DA, Li G, Blazenovic I, Lastra RR, Curtis M, Yamada SD, Perets R, McGregor SM, Andrade J, Fiehn O, Moellering RE, Mann M, Lengyel E (2019) Proteomics reveals NMMT as a master metabolic regulator of Cancer-associated fibroblasts. Nature 569(7758):723–728
Fadare O (2016) Diagnostic and molecular genetic pathology. In: Fadare O (ed) Precancerous lesions of the gynecologic tract, 1st edn. Springer, Cham
Fleszar AJ, Walker, A., Kreeger, PK, Notbohm, J (2019) Substrate curvature induces fallopian tube epithelial cell invasion via cell-cell tension in a model of ovarian cortical inclusion cysts. Integrative Biology
Fleszar AJ, Walker A, Porubsky V, Flanigan W, James D, Campagnola PJ, Weisman PS, Kreeger PK (2018) The extracellular matrix of ovarian cortical inclusion cysts modulates invasion of fallopian tube epithelial cells. APL Bioeng 2(3). https://doi.org/10.1063/1.5022595
Fogg KC, Olson WR, Miller JN, Khan A, Renner C, Hale I, Weisman PS, Kreeger PK (2019) Alternatively activated macrophage-derived secretome stimulates ovarian cancer spheroid spreading through a JAK2/STAT3 pathway. Cancer Lett 458:92–101. https://doi.org/10.1016/j.canlet.2019.05.029
Ghosh S, Albitar L, LeBaron R, Welch WR, Samimi G, Birrer MJ, Berkowitz RS, Mok SC (2010) Up-regulation of stromal versican expression in advanced stage serous ovarian cancer. Gynecol Oncol 119(1):114–120. https://doi.org/10.1016/j.ygyno.2010.05.029
Gubbels JA, Claussen N, Kapur AK, Connor JP, Patankar MS (2010) The detection, treatment, and biology of epithelial ovarian cancer. J Ovarian Res 3:8. https://doi.org/10.1186/1757-2215-3-8
Gurler H, Yu Y, Choi J, Kajdacsy-Balla AA, Barbolina MV (2015) Three-dimensional collagen type I matrix up-regulates nuclear isoforms of the microtubule associated protein tau implicated in resistance to paclitaxel therapy in ovarian carcinoma. Int J Mol Sci 16(2):3419–3433
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. https://doi.org/10.1016/j.cell.2011.02.013
Hoda MA, Rozsas A, Lang E, Klikovits T, Lohinai Z, Torok J, Bendek M, Berger W, Hegedus B, Klepetko W, Renyi-Vamos F, Grusch M, Dome B, Laszlo V (2016) High circulating activin a level is associated with tumor progression and predicts poor prognosis in lung adenocarcinoma. Oncotarget 7(12):13388–13399
Horikawa N, Abiko K, Matsumura N, Hamanishi J, Baba T, Yamaguchi K, Yoshioka Y, Koshiyama M, Konishi I (2017) Expression of vascular endothelial growth factor in ovarian Cancer inhibits tumor immunity through the accumulation of myeloid-derived suppressor cells. Clin Cancer Res 23(2):587–599. https://doi.org/10.1158/1078-0432.CCR-16-0387
Hsu CF, Huang HS, Chen PC, Ding DC, Chu TY (2019) IGF-axis confers transformation and regeneration of fallopian tube fimbria epithelium upon ovulation. EBioMedicine 41:597–609. https://doi.org/10.1016/j.ebiom.2019.01.061
Huang HS, Chu SC, Hsu CF, Chen PC, Ding DC, Chang MY, Chu TY (2015) Mutagenic, surviving and tumorigenic effects of follicular fluid in the context of p53 loss: initiation of fimbria carcinogenesis. Carcinogenesis 36(11):1419–1428. https://doi.org/10.1093/carcin/bgv132
Huang HS, Hsu CF, Chu SC, Chen PC, Ding DC, Chang MY, Chu TY (2016) Haemoglobin in pelvic fluid rescues fallopian tube epithelial cells from reactive oxygen species stress and apoptosis. J Pathol 240(4):484–494. https://doi.org/10.1002/path.4807
Huang D, Song SJ, Wu ZZ, Wu W, Cui XY, Chen JN, Zeng MS, Su SC (2017) Epstein-Barr virus-induced VEGF and CM-CSF drive nasopharyngeal carcinoma metastasis via recruitment and activation of macrophages. Cancer Res 77(13):3591–3604
Hyler AR, Baudoin NC, Brown MS, Stremler MA, Cimini D, Davalos RV, Schmelz EM (2018) Fluid shear stress impacts ovarian cancer cell viability, subcellular organization, and promotes genomic instability. PLoS One 13(3):e0194170
Irving-Rodgers HF, Rodgers RJ (2006) Extracellular matrix of the developing ovarian follicle. Semin Reprod Med 24(4):195–203. https://doi.org/10.1055/s-2006-948549
Januchowski R, Zawierucha P, Rucinski M, Nowicki M, Zabel M (2014) Extracellular matrix proteins expression profiling in chemoresistant variants of the A2780 ovarian cancer cell line. Biomed Res Int 2014(365867)
Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y, Crum CP (2008) Serous carcinogenesis in the fallopian tube: a descriptive classification. Int J Gynecol Pathol 27(1):1–9. https://doi.org/10.1097/pgp.0b013e31814b191f
John B, Naczki C, Patel C, Ghoneum A, Qasem S, Salih Z, Said N (2019) Regulation of the bi-directional cross-talk between ovarian Cancer cells and adipocytes by SPARC. Oncogene 38(22):4366–4383
Kalluri R (2016) The biology and function of fibroblasts in Cancer. Nat Rev Cancer 16(9):582–598
Kashima H, Wu RC, Wang Y, Sinno AK, Miyamoto T, Shiozawa T, Wang TL, Fader AN, Shih Ie M (2015) Laminin C1 expression by uterine carcinoma cells is associated with tumor progression. Gynecol Oncol 139(2):338–344. https://doi.org/10.1016/j.ygyno.2015.08.025
Kenny HA, Kaur S, Coussens LM, Lengyel E (2008) The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J Clin Invest 118(4):1367–1379
King SM, Hilliard TS, Wu LY, Jaffe RC, Fazleabas AT, Burdette JE (2011) The impact of ovulation on fallopian tube epithelial cells: evaluating three hypotheses connecting ovulation and serous ovarian cancer. Endocr Relat Cancer 18(5):627–642. https://doi.org/10.1530/ERC-11-0107
Klymenko Y, Wates RB, Weiss-Bilka H, Lombard R, Liu Y, Campbell L, Kim O, Wagner D, Ravosa MJ, Stack MS (2018) Modeling the effect of ascites-induced compression on ovarian cancer multicellular aggregates. Dis Model Mech 11:dmm034199
Ko SY, Barengo N, Ladanyi A, Lee JS, Marini F, Lengyel E, Naora H (2012) HOXA9 promotes ovarian Cancer growth by stimulating Cancer-associated fibroblasts. J Clin Invest 122(10):3603–3617
Kreeger PK (2013) Using partial least squares regression to analyze cellular response data. Sci Signal 6(271):tr7. https://doi.org/10.1126/scisignal.2003849
Kreeger PK, Strong LE, Masters KM (2018) Engineering approaches to study cellular decision making. Annu Rev Biomed Eng 20:49–72. https://doi.org/10.1146/annurev-bioeng-062117-121011
Kreuzinger C, Geroldinger A, Smeets D, Braicu EI, Sehouli J, Koller J, Wolf A, Darb-Esfahani S, Joehrens K, Vergote I, Vanderstichele A, Boeckx B, Lambrechts D, Gabra H, Wisman GBA, Trillsch F, Heinze G, Horvat R, Polterauer S, Berns E, Theillet C, Cacsire Castillo-Tong D (2017) A complex network of tumor microenvironment in human high-grade serous ovarian Cancer. Clin Cancer Res 23(24):7621–7632
Kuczek DE, Larsen AMH, Thorseth ML, Carretta M, Kalvisa A, Siersbaek MS, Simoes AMC, Roslind A, Engelholm LH, Noessner E, Donia M, Svane IM, Straten PT, Grontved L, Madsen DH (2019) Collagen density regulates the activity of tumor-infiltrating T cells. J Immunother Cancer 7(1):68
Kuhn EK, Soslow RA, Han G, Sehdev AS, Morin PJ, Wang T, Shih I (2012) The diagnostic and biological implications of Laminin expression in serous tubal intraepithelial carcinoma. Am J Surg Pathol 36(12):1826–1834
Labidi-Galy SI, Papp E, Hallberg D, Niknafs N, Adleff V, Noe M, Bhattacharya R, Novak M, Jones S, Phallen J, Hruban CA, Hirsch MS, Lin DI, Schwartz L, Maire CL, Tille JC, Bowden M, Ayhan A, Wood LD, Scharpf RB, Kurman R, Wang TL, Shih IM, Karchin R, Drapkin R, Velculescu VE (2017) High grade serous ovarian carcinomas originate in the fallopian tube. Nat Commun 8(1):1093. https://doi.org/10.1038/s41467-017-00962-1
Ladanyi A, Mukherjee A, Kenny HA, Johnson A, Mitra AK, Sundaresan S, Nieman KM, Pascual G, Benitah SA, Montag A, Yamada SD, Abumrad NA, Lengyel E (2018) Adipocyte-induced CD36 expression drives ovarian Cancer progression and metastasis. Oncogene 47(17):2285–2301
Lan C, Huang X, Lin S, Huang H, Cai Q, Wan T, Lu J, Liu J (2013) Expression of M2-polarized macrophages is associated with poor prognosis for advanced epithelial ovarian Cancer. Technol Cancer Res Treat 12(3):259–267
Lau A, Kollara A, St John E, Tone AA, Virtanen C, Greenblatt EM, King WA, Brown TJ (2014) Altered expression of inflammation-associated genes in oviductal cells following follicular fluid exposure: implications for ovarian carcinogenesis. Exp Biol Med (Maywood) 239(1):24–32. https://doi.org/10.1177/1535370213508216
Lawicki S, Gacuta-Szumarska E, Bedkowska GE, Szmitkowski M (2012) Hematopoietic cytokines as tumor markers in gynecological malignancies. A multivariate analysis in epithelial ovarian Cancer patients. Growth Factors 30:357–366
LeBleu VS, Kalluri R (2018) A peek into Cancer-associated fibroblasts: origins, functions and translational impact. Dis Model Mech 11(4)
Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD, Crum CP (2007) A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 211(1):26–35. https://doi.org/10.1002/path.2091
Lee JY, Yoon JK, Kim B, Kim S, Kim MA, Lim H, Bang D, Song YS (2015) Tumor evolution and intratumor heterogeneity of an epithelial ovarian cancer investigated using next-generation sequencing. BMC Cancer 15:85. https://doi.org/10.1186/s12885-015-1077-4
Lee W, Ko SY, Mohamed MS, Kenny HA, Lengyel E, Naora H (2018) Neutrophils facilitate ovarian cancer premetastatic niche formation in the omentum. J Exp Med 216(1):176–194
Lengyel E, Burdette JE, Kenny HA, Matei D, Pilrose J, Haluska P, Nephew KP, Hales DB, Stack MS (2014) Epithelial ovarian cancer experimental models. Oncogene 33(28):3619–3633. https://doi.org/10.1038/onc.2013.321
Liang Y, Cao Q, Gao X, Du H (2017) Increased bone morphogenetic protein-6 in follicular fluid and granulosa cells may correlate with fertilization and embryo quality in humans. Exp Ther Med 14(2):1171–1176. https://doi.org/10.3892/etm.2017.4603
Lietard J, Musso O, Theret N, L’Helgoualc’h A, Campion JP, Yamada Y, Clement B (1997) Sp1-mediated transactivation of LamC1 promoter and coordinated expression of laminin-gamma1 and Sp1 in human hepatocellular carcinomas. Am J Pathol 151(6):1663–1672
Lin EY, Nguyen AV, Russell RG, Pollard JW (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 193(6):727–740
Liu N, Ma Y, Li R, Jin H, Li M, Huang X, Feng HL, Qiao J (2012) Comparison of follicular fluid amphiregulin and EGF concentrations in patients undergoing IVF with different stimulation protocols. Endocrine 42(3):708–716. https://doi.org/10.1007/s12020-012-9706-z
Loessner D, Stok KS, Lutolf MP, Hutmacher DW, Clements JA, Rizzi SC (2010) Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials 31(32):8494–8506
Lyons RA, Saridogan E, Djahanbakhch O (2006) The effect of ovarian follicular fluid and peritoneal fluid on fallopian tube ciliary beat frequency. Hum Reprod 21(1):52–56. https://doi.org/10.1093/humrep/dei306
McKenzie AJ, Hicks SR, Svec KV, Naughton H, Edmunds ZL, Howe AK (2018) The mechanical microenvironment regulates ovarian cancer cell morphology, migration, and spheroid disaggregation. Sci Rep 8(1):7228
Moser TL, Pizzo SV, Bafetti LM, Fishman DA, Stack MS (1996) Evidence for preferential adhesion of ovarian epithelial carcinoma cells to type I collagen mediated by the alpha2beta1 integrin. Int J Cancer 67(5):695–701
Naba A, Pearce OMT, Del Rosario A, M D, Ding H, Rajeeve V, Cutillas PR, Balkwill FR, Hynes RO (2017) Characterization of the extracellular matrix of Normal and diseased tissues using proteomics. J Proteome Res 16(8):3083–3091
Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt MR, Romero IL, Carey MS, Mills GB, Hotamisligil GS, Yamada SD, Peter ME, Gwin K, Lengyel E (2011) Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 17(11):1498–1503
Obermueller E, Vosseler S, Fusenig NE, Mueller MM (2004) Cooperative autocrine and paracrine functions of granulocyte Colony-stimulating factor and granulocyte-macrophage Colony-stimulating factor in the progression of skin carcinoma cells. Cancer Res 64(21):7801–7812
Pearce OMT, Delaine-Smith RM, Maniati E, Nichols S, Wang J, Bohm S, Rajeeve V, Ullah D, Chakravarty P, Jones RR, Montfort A, Dowe T, Gribben J, Jones JL, Kocher HM, Serody JS, Vincent BG, Connelly J, Brenton JD, Chelala C, Cutillas PR, Lockley M, Bessant C, Knight MM, Balkwill FR (2018) Deconstruction of a metastatic tumor microenvironment reveals a common matrix response in human cancers. Cancer Discov 8(3):304–319
Perets R, Wyant GA, Muto KW, Bijron JG, Poole BB, Chin KT, Chen JY, Ohman AW, Stepule CD, Kwak S, Karst AM, Hirsch MS, Setlur SR, Crum CP, Dinulescu DM, Drapkin R (2013) Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell 24(6):751–765. https://doi.org/10.1016/j.ccr.2013.10.013
Platell C, Cooper D, Papdimitriou JM, Hall JC (2000) The omentum. World J Gastroenterol 6(2):169–176
Prasasya RP, Tian D, Kreeger PK (2011) Analysis of cancer signaling networks by systems biology to develop therapies. Semin Cancer Biol 21(3):200–206. https://doi.org/10.1016/j.semcancer.2011.04.001
Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR (2012) Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21(3):418–429
Purdie DM, Bain CJ, Siskind V, Webb PM, Green AC (2003) Ovulation and risk of epithelial ovarian cancer. Int J Cancer 104(2):228–232. https://doi.org/10.1002/ijc.10927
Rizvi I, Gurkan UA, Tasoglu S, Alagic N, Celli JP, Mensah LB, Mai Z, Demirci U, Hasan T (2013) Flow induces epithelial-mesenchymal transition, cellular heterogeneity and biomarker modulation in 3D ovarian cancer nodules. Proc Natl Acad Sci U S A 110(22):E1974–E1983
Shen Y, Shen R, Ge L, Zhu Q, Li F (2012) Fibrillar type I collagen matrices enhance metastasis/invasion of ovarian epithelial cancer via β1 integrin and PTEN signals. Int J Gynecol Cancer 22(8):1316–1324
Stanske M, Wienert S, Castillo-Tong DC, Kreuzinger C, Vergote I, Lambrechts S, Gabra H, Gourley C, Ganapathi RN, Kolaschinski I, Budczies J, Sehouli J, Ruscito I, Denkert C, Kulbe H, Schmitt W, Joehrens K, Braicu I, Darb-Esfahani S (2018) Dynamics of the Intratumoral immune response during progression of high-grade serous ovarian Cancer. Neoplasia 20(3):280–288
Sterzynska K, Klejewski A, Wojtowicz K, Swierczewska M, Nowacka M, Kazmierczak D, Andrezejewska M, Rusek D, Brazert M, Brazert J, Nowicki M, Januchowski R (2018) Mutual expression of ALDH1A1, LOX, and collagens in ovarian Cancer cell lines as combined CSCs- and ECM-related models of drug resistance development. Int J Mol Sci 20(1)
Tang J, Pulliam N, Ozes A, Buechlein A, D N, Keer H, Rusch D, O’Hagan H, Stack MS, Nephew KP (2018) Epigenetic targeting of adipocytes inhibits high-grade serous ovarian Cancer cell migration and invasion. Mol Cancer Res 16(8):1226–1240
ten Dam GB, van de Westerlo EM, Purushothaman A, Stan RV, Bulten J, Sweep FC, Massuger LF, Sugahara K, van Kuppevelt TH (2007) Antibody GD3G7 selected against embryonic glycosaminoglycans defines chondroitin sulfate-E domains highly up-regulated in ovarian cancer and involved in vascular endothelial growth factor binding. Am J Pathol 171(4):1324–1333. https://doi.org/10.2353/ajpath.2007.070111
Tian D, Kreeger PK (2014) Analysis of the quantitative balance between insulin-like growth factor (IGF)-1 ligand, receptor, and binding protein levels to predict cell sensitivity and therapeutic efficacy. BMC Syst Biol 8(98):1752–0509
Tian D, Mitchell I, Kreeger PK (2016) Quantitative analysis of insulin-like growth factor 2 receptor and insulin-like growth factor binding proteins to identify control mechanisms for insulin-like growth factor 1 receptor phosphorylation. BMC Syst Biol 10:15. https://doi.org/10.1186/s12918-016-0263-6
Tilbury KB, Campbell KR, Eliceiri KW, Salih SM, Patankar M, Campagnola PJ (2017) Stromal alterations in ovarian cancers via wavelength dependent second harmonic generation microscopy and optical scattering. BMC Cancer 17(1):102. https://doi.org/10.1186/s12885-017-3090-2
Vallen MJ, Massuger LF, ten Dam GB, Bulten J, van Kuppevelt TH (2012) Highly sulfated chondroitin sulfates, a novel class of prognostic biomarkers in ovarian cancer tissue. Gynecol Oncol 127(1):202–209. https://doi.org/10.1016/j.ygyno.2012.06.022
Vallen MJ, Schmidt S, Oosterhof A, Bulten J, Massuger LF, van Kuppevelt TH (2014) Primary ovarian carcinomas and abdominal metastasis contain 4,6-disulfated chondroitin sulfate rich regions, which provide adhesive properties to tumour cells. PLoS One 9(11):e111806. https://doi.org/10.1371/journal.pone.0111806
van der Steen SC, van Tilborg AA, Vallen MJ, Bulten J, van Kuppevelt TH, Massuger LF (2016) Prognostic significance of highly sulfated chondroitin sulfates in ovarian cancer defined by the single chain antibody GD3A11. Gynecol Oncol 140(3):527–536. https://doi.org/10.1016/j.ygyno.2015.12.024
van der Steen S, Bulten J, Van de Vijver KK, van Kuppevelt TH, Massuger L (2017) Changes in the extracellular matrix are associated with the development of serous tubal intraepithelial carcinoma into high-grade serous carcinoma. Int J Gynecol Cancer 27(6):1072–1081. https://doi.org/10.1097/IGC.0000000000000933
Visvanathan K, Vang R, Shaw P, Gross A, Soslow R, Parkash V, Shih Ie M, Kurman RJ (2011) Diagnosis of serous tubal intraepithelial carcinoma based on morphologic and immunohistochemical features: a reproducibility study. Am J Surg Pathol 35(12):1766–1775. https://doi.org/10.1097/PAS.0b013e31822f58bc
Wang R, Zhang T, Ma Z, Wang Y, Cheng Z, Xu H, Li W, Wang X (2010) The interaction of coagulation factor XII and monocyte/macrophages mediating peritoneal metastasis of epithelial ovarian cancer. Gynecol Oncol 117(3):460–466
Ween MP, Hummitzsch K, Rodgers RJ, Oehler MK, Ricciardelli C (2011) Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides. Clin Exp Metastasis 28(2):113–125. https://doi.org/10.1007/s10585-010-9363-7
Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J, Condeelis J (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64(19):7022–7029
Yang Z, Yang X, Xu S, Jin P, Li X, Wei X, Liu D, Huang K, Long S, Wang Y, Sun C, Chen G, Hu J, Meng L, Ma D, Gao Q (2017) Reprogramming of stromal fibroblasts by SNAI2 contributes to tumor Desmoplasia and ovarian Cancer progression. Mol Cancer 16(1):163
Yang-Hartwich Y, Gurrea-Soteras M, Sumi N, Joo WD, Holmberg JC, Craveiro V, Alvero AB, Mor G (2014) Ovulation and extra-ovarian origin of ovarian cancer. Sci Rep 4:6116. https://doi.org/10.1038/srep06116
Zamah AM, Hassis ME, Albertolle ME, Williams KE (2015) Proteomic analysis of human follicular fluid from fertile women. Clin Proteomics 12(1):5. https://doi.org/10.1186/s12014-015-9077-6
Zhang T, Ma Z, Wang R, Wang Y, Wang S, Cheng Z, Xu H, Jin X, Li W, Wang X (2010) Thrombin facilitates invasion of ovarian cancer along peritoneum by inducing monocyte differentiation toward tumor-associated macrophage-like cells. Cancer Immunol Immunother 59(7):1097–1108
Zhang Y, Yan W, Chen X (2011) Mutant p53 disrupts MCF-10A cell polarity in three-dimensional culture via epithelial-to-mesenchymal transitions. J Biol Chem 286(18):16218–16228. https://doi.org/10.1074/jbc.M110.214585
Zink KE, Dean M, Burdette JE, Sanchez LM (2018) Imaging mass spectrometry reveals crosstalk between the fallopian tube and the ovary that drives primary metastasis of ovarian Cancer. ACS Cent Sci 4(10):1360–1370. https://doi.org/10.1021/acscentsci.8b00405
Acknowledgments
Funding was provided by grants to Pamela K. Kreeger from the NIH (1R01CA232517, 1R01CA240965, and 1R21CA227922), the American Cancer Society (133003-MBG-18-206-01-COUN), and a Pilot grant from the Rivkin Center for Ovarian Cancer.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Micek, H.M., Visetsouk, M.R., Fleszar, A.J., Kreeger, P.K. (2020). The Many Microenvironments of Ovarian Cancer. In: Birbrair, A. (eds) Tumor Microenvironments in Organs. Advances in Experimental Medicine and Biology, vol 1296. Springer, Cham. https://doi.org/10.1007/978-3-030-59038-3_12
Download citation
DOI: https://doi.org/10.1007/978-3-030-59038-3_12
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-59037-6
Online ISBN: 978-3-030-59038-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)