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Cancer Cell International
Published in: Cancer Cell International 1/2017

Open Access 01-12-2017 | Hypothesis

Cancer metastasis: enactment of the script for human reproductive drama

Authors: Xichun Sun, Xiwu Liu

Published in: Cancer Cell International | Issue 1/2017

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Abstract

Based on compelling evidence from many biological disciplines, we put forth a hypothesis for cancer metastasis. In the hypothesis, the metastatic cascade is depicted as human reproduction in miniature. Illustrated in a reproductive light, the staggering resemblance of cancer metastasis to human reproduction becomes evident despite some ostensible dis-similarities. In parallel to the appearance of primordial germ cells during early embryogenesis, the cancer reproductive saga starts with the separation of metastasis initiating cells (MICs) from cancer initiating cells when the primary cancer is still in its infancy. Prime MICs embark on a journey to the host bone marrow where they undergo further development and regulation. Migrating MICs are guided by the same CXCR4/CYCL12 axis as used in the migration of primordial germ cells to the genital ridge. Like the ovary, the host bone marrow features immune privileges, coolness, hypoxia and acidity which are essential for stemness maintenance and regulation. Opportune activation of the MICs via fusion with bone marrow stem cells triggers a frenzy of cellular proliferation and sets them on the move again. This scenario is akin to oocyte fertilization in the Fallopian tube and its subsequent journey towards the decidum. Just as the human reproductive process is plagued with undesirable outcomes so is the cancer metastasis highly inefficient. The climax of the cancer metastatic drama (colonization) is reached when proliferating MIC clusters attempt to settle down on decidum-like premetastatic sites. Successfully colonized clusters blossom into overt macrometastases only after the execution of sophisticated immunomodulation, angiogenesis and vascular remodeling. Similarly, the implanted blastomere needs to orchestrate these feats before flourishing into a new life. What is more, the cancer reproductive drama seems to be directed by a primordial hypothalamus–pituitary–gonad axis. Pursuing this reproductive trail could lead to new frontiers and breakthroughs in cancer research and therapeutics.
Literature
1.
Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331(6024):1559–64.PubMedCrossRef
2.
Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D, Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15(3):220–31.PubMedPubMedCentralCrossRef
3.
Ruegg C, Monnier Y, Kuonen F, Imaizumi N. Radiation-induced modifications of the tumor microenvironment promote metastasis. Bull Cancer. 2011;98(6):47–57.PubMed
4.
Daenen LG, Roodhart JM, van Amersfoort M, Dehnad M, Roessingh W, Ulfman LH, Derksen PW, Voest EE. Chemotherapy enhances metastasis formation via VEGFR-1-expressing endothelial cells. Cancer Res. 2011;71(22):6976–85.PubMedCrossRef
5.
Neeman E, Ben-Eliyahu S. Surgery and stress promote cancer metastasis: new outlooks on perioperative mediating mechanisms and immune involvement. Brain Behav Immun. 2013;30:S32–40.PubMedCrossRef
6.
7.
Seyfried TN, Huysentruyt LC. On the origin of cancer metastasis. Crit Rev Oncog. 2011;18(1–2):43–73.
8.
9.
Suzumori N, Sugiura-Ogasawara M. Genetic factors as a cause of miscarriage. Curr Med Chem. 2010;17(29):3431–7.PubMedCrossRef
10.
van den Berg MM, van Maarle MC, van Wely M, Goddijn M. Genetics of early miscarriage. Biochim Biophys Acta. 2012;1822(12):1951–9.PubMedCrossRef
11.
12.
Rull K, Nagirnaja L, Laan M. Genetics of recurrent miscarriage: challenges, current knowledge, future directions. Front Genet. 2011;3:34.
13.
Anousha N, Hossein-Nezhad A, Biramijamal F, Rahmani A, Maghbooli Z, Aghababaei E, Nemati S. Association study of estrogen receptor alpha gene polymorphisms with spontaneous abortion: is this a possible reason for unexplained spontaneous abortion? Biomed Res Int. 2013;2013:256470.PubMedPubMedCentralCrossRef
14.
15.
Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1(3):313–23.PubMedCrossRef
16.
Haffner MC, Mosbruger T, Esopi DM, Fedor H, Heaphy CM, Walker DA, Adejola N, Gurel M, Hicks J, Meeker AK, et al. Tracking the clonal origin of lethal prostate cancer. J Clin Invest. 2013;123(11):4918–22.PubMedPubMedCentralCrossRef
17.
Klein CA. Selection and adaptation during metastatic cancer progression. Nature. 2013;501(7467):365–72.PubMedCrossRef
18.
Ross JB, Huh D, Noble LB, Tavazoie SF. Identification of molecular determinants of primary and metastatic tumour re-initiation in breast cancer. Nat Cell Biol. 2014;17(5):651–64.CrossRef
19.
Jacob LS, Vanharanta S, Obenauf AC, Pirun M, Viale A, Socci ND, Massague J. Metastatic competence can emerge with selection of preexisting oncogenic alleles without a need of new mutations. Cancer Res. 2015;75(18):3713–9.PubMedPubMedCentralCrossRef
20.
21.
22.
Chow KH, Shin DM, Jenkins MH, Miller EE, Shih DJ, Choi S, Low BE, Philip V, Rybinski B, Bronson RT, et al. Epigenetic states of cells of origin and tumor evolution drive tumor-initiating cell phenotype and tumor heterogeneity. Cancer Res. 2014;74(17):4864–74.PubMedPubMedCentralCrossRef
23.
Cock-Rada A, Weitzman JB. The methylation landscape of tumour metastasis. Biol Cell. 2013;105(2):73–90.PubMedCrossRef
24.
Mudduluru G, Abba M, Batliner J, Patil N, Scharp M, Lunavat TR, Leupold JH, Oleksiuk O, Juraeva D, Thiele W, et al. A systematic approach to defining the microRNA landscape in metastasis. Cancer Res. 2015;75(15):3010–9.PubMedCrossRef
25.
Liu W, Vivian CJ, Brinker AE, Hampton KR, Lianidou E, Welch DR. Microenvironmental influences on metastasis suppressor expression and function during a metastatic cell’s journey. Cancer Microenviron. 2014;7(3):117–31.PubMedPubMedCentralCrossRef
26.
27.
28.
Hiden U, Bilban M, Knofler M, Desoye G. Kisspeptins and the placenta: regulation of trophoblast invasion. Rev Endocr Metab Disord. 2007;8(1):31–9.PubMedCrossRef
29.
Jabeen S, Qureshi MZ, Javed Z, Iqbal MJ, Ismail M, Farooqi AA. Kisspeptin mediated signaling in cancer. Curr Top Med Chem. 2016;16(22):2471–6.PubMedCrossRef
30.
Prabhu VV, Sakthivel KM, Guruvayoorappan C. Kisspeptins (KiSS-1): essential players in suppressing tumor metastasis. Asian Pac J Cancer Prev. 2013;14(11):6215–20.PubMedCrossRef
31.
Limonta P, Montagnani Marelli M, Mai S, Motta M, Martini L, Moretti RM. GnRH receptors in cancer: from cell biology to novel targeted therapeutic strategies. Endocr Rev. 2013;33(5):784–811.CrossRef
32.
Aguilar-Rojas A, Huerta-Reyes M. Human gonadotropin-releasing hormone receptor-activated cellular functions and signaling pathways in extra-pituitary tissues and cancer cells (Review). Oncol Rep. 2009;22(5):981–90.PubMedCrossRef
33.
Govindaraj V, Arya SV, Rao AJ. Differential action of glycoprotein hormones: significance in cancer progression. Horm Cancer. 2014;5(1):1–10.PubMedCrossRef
34.
Radu A, Pichon C, Camparo P, Antoine M, Allory Y, Couvelard A, Fromont G, Hai MT, Ghinea N. Expression of follicle-stimulating hormone receptor in tumor blood vessels. N Engl J Med. 2010;363(17):1621–30.PubMedCrossRef
35.
Cole LA. HCG variants, the growth factors which drive human malignancies. Am J Cancer Res. 2012;2(1):22–35.PubMed
36.
37.
Munoz J, Wheler J, Kurzrock R. Expression of estrogen and progesterone receptors across human malignancies: new therapeutic opportunities. Cancer Metastasis Rev. 2014;34(4):547–61.CrossRef
38.
Siegfried JM, Stabile LP. Estrongenic steroid hormones in lung cancer. Semin Oncol. 2014;41(1):5–16.PubMedCrossRef
39.
Folkerd EJ, Dowsett M. Influence of sex hormones on cancer progression. J Clin Oncol. 2010;28(26):4038–44.PubMedCrossRef
40.
Prithviraj P, Anaka M, McKeown SJ, Permezel M, Walkiewicz M, Cebon J, Behren A, Jayachandran A. Pregnancy associated plasma protein-A links pregnancy and melanoma progression by promoting cellular migration and invasion. Oncotarget. 2015;6(18):15953–65.PubMedPubMedCentralCrossRef
41.
Dewerchin M, Carmeliet P. Placental growth factor in cancer. Expert Opin Ther Targets. 2014;18(11):1339–54.PubMedCrossRef
42.
Szekeres-Bartho J, Polgar B. PIBF: the double edged sword. Pregnancy and tumor. Am J Reprod Immunol. 2010;64(2):77–86.PubMed
43.
Chen J, Wang J, Shao J, Gao Y, Xu J, Yu S, Liu Z, Jia L. The unique pharmacological characteristics of mifepristone (RU486): from terminating pregnancy to preventing cancer metastasis. Med Res Rev. 2014;34(5):979–1000.PubMedCrossRef
44.
Bernard V, Young J, Chanson P, Binart N. New insights in prolactin: pathological implications. Nat Rev Endocrinol. 2015;11(5):265–75.PubMedCrossRef
45.
Strunecka A, Hynie S, Klenerova V. Role of oxytocin/oxytocin receptor system in regulation of cell growth and neoplastic processes. Folia Biol (Praha). 2009;55(5):159–65.
46.
Grusch M, Drucker C, Peter-Vorosmarty B, Erlach N, Lackner A, Losert A, Macheiner D, Schneider WJ, Hermann M, Groome NP, et al. Deregulation of the activin/follistatin system in hepatocarcinogenesis. J Hepatol. 2006;45(5):673–80.PubMedCrossRef
47.
Le Bras GF, Loomans HA, Taylor CJ, Revetta FL, Andl CD. Activin A balance regulates epithelial invasiveness and tumorigenesis. Lab Invest. 2014;94(10):1134–46.PubMedPubMedCentralCrossRef
48.
49.
Abdelbaset-Ismail A, Suszynska M, Borkowska S, Adamiak M, Ratajczak J, Kucia M, Ratajczak MZ. Human haematopoietic stem/progenitor cells express several functional sex hormone receptors. J Cell Mol Med. 2016;20(1):134–46.PubMedCrossRef
50.
Virant-Klun I. Very small embryonic-like stem cells: a potential developmental link between germinal lineage and hematopoiesis in humans. Stem Cells Dev. 2016;25(2):101–13.PubMedCrossRef
51.
Suszynska M, Poniewierska-Baran A, Gunjal P, Ratajczak J, Marycz K, Kakar SS, Kucia M, Ratajczak MZ. Expression of the erythropoietin receptor by germline-derived cells-further support for a potential developmental link between the germline and hematopoiesis. J Ovarian Res. 2014;7:66.PubMedPubMedCentralCrossRef
52.
Alameddine RS, Hamieh L, Shamseddine A. From sprouting angiogenesis to erythrocytes generation by cancer stem cells: evolving concepts in tumor microcirculation. Biomed Res Int. 2014;2014:986768.PubMedPubMedCentralCrossRef
53.
Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40(5):499–507.PubMedPubMedCentralCrossRef
54.
Cojoc M, Peitzsch C, Trautmann F, Polishchuk L, Telegeev GD, Dubrovska A. Emerging targets in cancer management: role of the CXCL12/CXCR4 axis. Onco Targets Ther. 2013;6:1347–61.PubMedPubMedCentral
55.
Cirello V, Fugazzola L. Novel insights into the link between fetal cell microchimerism and maternal cancers. J Cancer Res Clin Oncol. 2016;142(8):1697–704.PubMedCrossRef
56.
Al-Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med. 2000;6(1):100–2.PubMedCrossRef
57.
Cheung KJ, Ewald AJ. A collective route to metastasis: seeding by tumor cell clusters. Science. 2016;352(6282):167–9.PubMedCrossRef
58.
Sceneay J, Smyth MJ, Moller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32(3–4):449–64.PubMedCrossRef
59.
Zoccoli A, Iuliani M, Pantano F, Imperatori M, Intagliata S, Vincenzi B, Marchetti P, Papapietro N, Denaro V, Tonini G, et al. Premetastatic niche: ready for new therapeutic interventions? Expert Opin Ther Targets. 2012;16(Suppl 2):S119–29.PubMedCrossRef
60.
Fridman WH, Remark R, Goc J, Giraldo NA, Becht E, Hammond SA, Damotte D, Dieu-Nosjean MC, Sautes-Fridman C. The immune microenvironment: a major player in human cancers. Int Arch Allergy Immunol. 2014;164(1):13–26.PubMedCrossRef
61.
Fenelon JC, Banerjee A, Murphy BD. Embryonic diapause: development on hold. Int J Dev Biol. 2014;58(2–4):163–74.PubMedCrossRef
62.
Renfree MB, Shaw G. Embryo-endometrial interactions during early development after embryonic diapause in the marsupial tammar wallaby. Int J Dev Biol. 2014;58(2–4):175–81.PubMedCrossRef
63.
64.
65.
Fenelon JC, Shaw G, O’Neill C, Frankenberg S, Renfree MB. Paf receptor expression in the marsupial embryo and endometrium during embryonic diapause. Reproduction. 2014;147(1):21–31.PubMedCrossRef
66.
Amelio I, Melino G. The p53 family and the hypoxia-inducible factors (HIFs): determinants of cancer progression. Trends Biochem Sci. 2015;40(8):425–34.PubMedCrossRef
67.
Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12(4):298–306.PubMedCrossRef
68.
Holtan SG, Creedon DJ, Haluska P, Markovic SN. Cancer and pregnancy: parallels in growth, invasion, and immune modulation and implications for cancer therapeutic agents. Mayo Clin Proc. 2009;84(11):985–1000.PubMedPubMedCentralCrossRef
69.
Beaman KD, Jaiswal MK, Katara GK, Kulshreshta A, Pamarthy S, Ibrahim S, Kwak-Kim J, Gilman-Sachs A. Pregnancy is a model for tumors, not transplantation. Am J Reprod Immunol. 2016;76(1):3–7.PubMedCrossRef
70.
Carosella ED, Rouas-Freiss N, Roux DT, Moreau P, LeMaoult J. HLA-G: an immune checkpoint molecule. Adv Immunol. 2015;127:33–144.PubMedCrossRef
71.
Chiang WF, Liu SY, Fang LY, Lin CN, Wu MH, Chen YC, Chen YL, Jin YT. Overexpression of galectin-1 at the tumor invasion front is associated with poor prognosis in early-stage oral squamous cell carcinoma. Oral Oncol. 2008;44(4):325–34.PubMedCrossRef
72.
Boucher LD, Yoneda K. The expression of trophoblastic cell markers by lung carcinomas. Hum Pathol. 1995;26(11):1201–6.PubMedCrossRef
73.
Li D, Wen X, Ghali L, Al-Shalabi FM, Docherty SM, Purkis P, Iles RK. hCG beta expression by cervical squamous carcinoma–in vivo histological association with tumour invasion and apoptosis. Histopathology. 2008;53(2):147–55.PubMedCrossRef
74.
Thijssen VL, Heusschen R, Caers J, Griffioen AW. Galectin expression in cancer diagnosis and prognosis: a systematic review. Biochim Biophys Acta. 2015;1855(2):235–47.PubMed
75.
Guo P, Fu BM. Effect of wall compliance and permeability on blood-flow rate in counter-current microvessels formed from anastomosis during tumor-induced angiogenesis. J Biomech Eng. 2012;134(4):041003.PubMedCrossRef
76.
Meehan B, Dombrovsky A, Magnus N, Rak J. Arteriogenic expansion of extratumoral macrovessels-impact of vascular ageing. Neoplasma. 2014;62(3):372–83.CrossRef
77.
78.
Chaligne R, Heard E. X-chromosome inactivation in development and cancer. FEBS Lett. 2014;588(15):2514–22.PubMedCrossRef
79.
80.
81.
Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31(Suppl):S33–9.PubMedCrossRef
82.
Serrano A, Castro-Vega I, Redondo M. Role of gene methylation in antitumor immune response: implication for tumor progression. Cancers (Basel). 2011;3(2):1672–90.PubMedCentralCrossRef
83.
Naxerova K, Jain RK. Using tumour phylogenetics to identify the roots of metastasis in humans. Nat Rev Clin Oncol. 2015;12(5):258–72.PubMedCrossRef
84.
Wu GJ, Dickerson EB. Frequent and increased expression of human METCAM/MUC18 in cancer tissues and metastatic lesions is associated with the clinical progression of human ovarian carcinoma. Taiwan J Obstet Gynecol. 2014;53(4):509–17.PubMedCrossRef
85.
Lin JC, Chiang CF, Wang SW, Wang WY, Kwan PC, Wu GJ. Significance of expression of human METCAM/MUC18 in nasopharyngeal carcinomas and metastatic lesions. Asian Pac J Cancer Prev. 2014;15(1):245–52.PubMedCrossRef
86.
Siraj A, Desestret V, Antoine M, Fromont G, Huerre M, Sanson M, Camparo P, Pichon C, Planeix F, Gonin J, et al. Expression of follicle-stimulating hormone receptor by the vascular endothelium in tumor metastases. BMC Cancer. 2013;13:246.PubMedPubMedCentralCrossRef
87.
Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J. Tumor self-seeding by circulating cancer cells. Cell. 2009;139(7):1315–26.PubMedPubMedCentralCrossRef
88.
Yamauchi H, Suto T, Kigure W, Morita H, Kato T, Yajima R, Fujii T, Yamaguchi S, Tsutsumi S, Asao T, et al. The progression potential of peritoneal dissemination nodules from gastrointestinal tumors. Int Surg. 2011;96(4):352–7.PubMedCrossRef
89.
Falato C, Lorent J, Tani E, Karlsson E, Wright PK, Bergh J, Foukakis T. Ki67 measured in metastatic tissue and prognosis in patients with advanced breast cancer. Breast Cancer Res Treat. 2014;147(2):407–14.PubMedCrossRef
90.
Gallaher J, Babu A, Plevritis S, Anderson AR. Bridging population and tissue scale tumor dynamics: a new paradigm for understanding differences in tumor growth and metastatic disease. Cancer Res. 2014;74(2):426–35.PubMedPubMedCentralCrossRef
91.
Yap KL, Hafez MJ, Mao TL, Kurman RJ, Murphy KM, Shih Ie M. Lack of a y-chromosomal complement in the majority of gestational trophoblastic neoplasms. J Oncol. 2010;2010:364508.PubMedPubMedCentralCrossRef
92.
Nakamura TJ, Sellix MT, Kudo T, Nakao N, Yoshimura T, Ebihara S, Colwell CS, Block GD. Influence of the estrous cycle on clock gene expression in reproductive tissues: effects of fluctuating ovarian steroid hormone levels. Steroids. 2010;75(3):203–12.PubMedPubMedCentralCrossRef
93.
Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod. 2010;16(5):297–310.PubMedCrossRef
94.
Sutherland RL, Prall OW, Watts CK, Musgrove EA. Estrogen and progestin regulation of cell cycle progression. J Mammary Gland Biol Neoplasia. 1998;3(1):63–72.PubMedCrossRef
95.
96.
Comitato R, Saba A, Turrini A, Arganini C, Virgili F. Sex hormones and macronutrient metabolism. Crit Rev Food Sci Nutr. 2015;55(2):227–41.PubMedCrossRef
97.
Arck P, Hansen PJ, Mulac Jericevic B, Piccinni MP, Szekeres-Bartho J. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am J Reprod Immunol. 2007;58(3):268–79.PubMedCrossRef
98.
Park MK, Kanaho Y, Enomoto M. Regulation of the cell proliferation and migration as extra-pituitary functions of GnRH. Gen Comp Endocrinol. 2013;181:259–64.PubMedCrossRef
99.
100.
101.
Wetendorf M, DeMayo FJ. Progesterone receptor signaling in the initiation of pregnancy and preservation of a healthy uterus. Int J Dev Biol. 2014;58(2–4):95–106.PubMedPubMedCentralCrossRef
102.
Wetendorf M, DeMayo FJ. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol Cell Endocrinol. 2012;357(1–2):108–18.PubMedCrossRef
103.
Holzel D, Eckel R, Emeny RT, Engel J. Distant metastases do not metastasize. Cancer Metastasis Rev. 2010;29(4):737–50.PubMedCrossRef
104.
Engel J, Emeny RT, Holzel D. Positive lymph nodes do not metastasize. Cancer Metastasis Rev. 2012;31(1–2):235–46.PubMedCrossRef
105.
Bartosch C, Monteiro-Reis S, Vieira R, Pereira A, Rodrigues M, Jeronimo C, Lopes JM. Endometrial endometrioid carcinoma metastases show decreased er-alpha and pr-a expression compared to matched primary tumors. PLoS ONE. 2015;10(8):e0134969.PubMedPubMedCentralCrossRef
106.
Curtit E, Nerich V, Mansi L, Chaigneau L, Cals L, Villanueva C, Bazan F, Montcuquet P, Meneveau N, Perrin S, et al. Discordances in estrogen receptor status, progesterone receptor status, and HER2 status between primary breast cancer and metastasis. Oncologist. 2013;18(6):667–74.PubMedPubMedCentralCrossRef
107.
Micheli A, Ciampichini R, Oberaigner W, Ciccolallo L, de Vries E, Izarzugaza I, Zambon P, Gatta G, De Angelis R. The advantage of women in cancer survival: an analysis of EUROCARE-4 data. Eur J Cancer. 2009;45(6):1017–27.PubMedCrossRef
108.
Joosse A, Collette S, Suciu S, Nijsten T, Lejeune F, Kleeberg UR, Coebergh JW, Eggermont AM, de Vries E. Superior outcome of women with stage I/II cutaneous melanoma: pooled analysis of four European Organisation for Research and Treatment of Cancer phase III trials. J Clin Oncol. 2012;30(18):2240–7.PubMedCrossRef
109.
Jensen LD. The circadian clock and hypoxia in tumor cell de-differentiation and metastasis. Biochim Biophys Acta. 2014;1850(8):1633–41.PubMedCrossRef
110.
111.
Van Acker HH, Anguille S, Willemen Y, Smits EL, Van Tendeloo VF. Bisphosphonates for cancer treatment: mechanisms of action and lessons from clinical trials. Pharmacol Ther. 2016;158:24–40.PubMedCrossRef
112.
Iversen L, Sivasubramaniam S, Lee AJ, Fielding S, Hannaford PC. Lifetime cancer risk and combined oral contraceptives: the Royal College of General Practitioners’ Oral Contraception Study. Am J Obstet Gynecol. 2017. doi:10.​1016/​j.​ajog.​2017.​02.​002.PubMed
Metadata
Title
Cancer metastasis: enactment of the script for human reproductive drama
Authors
Xichun Sun
Xiwu Liu
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2017
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-017-0421-y

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