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Etiology and Pathogenesis of Epithelial Ovarian Cancer

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Etiology and Pathogenesis of Epithelial Ovarian Cancer Etiology and Pathogenesis of Epithelial Ovarian Cancer The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Mok, Samuel C., Joseph Kwong, William R. Welch, Goli Samimi, Laurent Ozbun, Tomas Bonome, Michael J. Birrer, Ross S. Berkowitz, and Kwong-Kwok Wong. 2007. “Etiology and Pathogenesis of Epithelial Ovarian Cancer.” Disease Markers 23 (5-6): 367-376. doi:10.1155/2007/474320. http:// dx.doi.org/10.1155/2007/474320. Published Version doi:10.1155/2007/474320 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:11879312 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Disease Markers 23 (2007) 367–376 367 IOS Press Etiology and pathogenesis of epithelial ovarian cancer Samuel C. Moka,b,∗, Joseph Kwonga, William R. Welchc, Goli Samimid,e, Laurent Ozbund, Tomas Bonomed, Michael J. Birrerd, Ross S. Berkowitza,b and Kwong-Kwok Wongf aDepartment of Obstetrics, Gynecology, and Reproductive Biology, Laboratory of Gynecologic Oncology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA bGillette Center For Women’s Cancer, Dana-Farber/Harvard Cancer Center, Boston, MA 02115, USA cDepartment of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115 USA dCell and Cancer Biology Branch, Center for Cancer Research, National Cancer Institute, Bethesda, MD 20892, USA eCancer Prevention Fellowship Program, Office of Preventative Oncology, Division of Cancer Prevention, Bethesda, MD 20892, USA f Department of Gynecologic Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA Abstract. Ovarian cancer is complex disease composed of different histological grades and types. However, the underlying molecular mechanisms involved in the development of different phenotypes remain largely unknown. Epidemiological studies identified multiple exogenous and endogenous risk factors for ovarian cancer development. Among them, an inflammatory stromal microenvironment seems to play a critical role in the initiation of the disease. The interaction between such a microenvironment, genetic polymorphisms, and different epithelial components such as endosalpingiosis, endometriosis, and ovarian inclusion cyst in the ovarian cortex may induce different genetic changes identified in the epithelial component of different histological types of ovarian tumors. Genetic studies on different histological grades and types provide insight into the pathogenetic pathways for the development of different disease phenotypes. However, the link between all these genetic changes and the etiological factors remains to be established. Keywords: Ovarian cancer, microenvironment, inflammation, pathogenesis 1. Introduction the ovaries [2]. The human ovarian surface epithelium (HOSE) is believed to originate from the mesothelium Ovarian cancer kills more American women than any of the embryonic gonad (the mullerian epithelium). In other gynecologic cancer and is, for the same group, the contrast to colorectal cancer, ovarian cancer does not fifth most common cause of cancer-related death [1]. have well-defined precursor lesions. It has more com- Although all human ovary cells, including epithelial, plex histological features and early stage cancer sam- stromal, and germ cells, may undergo neoplastic trans- ples are more difficult to obtain. These differences lim- formation, 80% to 90% of malignant ovarian tumors it our ability to identify risk factors, which are impor- come from the single layer of epithelial cells covering tant for the pathogenesis of ovarian cancer. In the last decade, multiple endogenous and exogenous risk fac- ∗ tors as well as genetic alterations have been identified Corresponding author: Samuel C. Mok, Laboratory of Gyne- for ovarian cancer. In this review, we will summarize cologic Oncology, Brigham and Women’s Hospital, BLI-447, 221 Longwood Avenue, Boston, MA 02115, USA. Tel.: +1 617 278 some of these risk factors and genetic changes identi- 1096; Fax: +1 617 9750818; E-mail: [email protected]. fied for all or specific histological types of ovarian can- ISSN 0278-0240/07/$17.00 2007 – IOS Press and the authors. All rights reserved 368 S.C. Mok et al. / Etiology and pathogenesis of epithelial ovarian cancer cer, which may provide insights into the development have shown an increased incidence of ovarian cancer in of the disease. women who are nulliparous, have had fewer pregnan- cies, have never breast-fed, or are infertileother condi- tions that may increase the number of ovulations in a 2. Histology woman’s lifetime [4,6–8]. The apparent overall relationship between ovulations Epithelial ovarian tumors are classified as benign, history and risk has prompted the development of sev- low malignant potential (borderline), or malignant ac- eral unified hypotheses of ovarian cancer pathogenesis. cording to the World Health Organization (WHO) cri- teria [3]. Benign epithelium is characterized by a sin- 3.1. Hypothesis 1 gle or minimally stratified layer of cells. These cells are columnar and often ciliated in serous tumors and In the earliest of these, it was postulated that “inces- contain abundant apical cytoplasmic mucin in muci- sant ovulation” leads to neoplastic transformation of nous tumors. Atypical epithelium lining of borderline HOSE cells [9,10]. This hypothesis states that every or low malignant potential (LMP) tumor is character- ovulation creates a wound that HOSE cells repair by ized by cellular proliferation and pleomorphism with- undergoing postovulation mitosis and proliferation and out stromal invasion. Malignant epithelium demon- that the increase in cell proliferation increases the like- strates marked atypia, increased mitotic activity, and lihood that age- or toxin-caused aberrations in DNA stromal invasion. Although the histopathologic fea- repair mechanisms will permit genetic damage to go tures of ovarian tumors vary substantially, all tumors unrepaired and become potentially carcinogenic muta- exhibit characteristics similar to those of the mullerian tions [11–14]. Several studies have found evidence that epithelium [4]. There are four major histological types supports the incessant ovulation hypothesis. In one, the of ovarian cancer. Serous tumors are the most common repeated subculture of rat ovarian surface epithelium form of ovarian neoplasm with epithelial cells resem- (OSE) cells induced spontaneous cellular transforma- bling those of the fallopian tube. They comprise about tion and chromosomal aberrations [15,16]. In anoth- 50–60% of primary epithelial ovarian tumors. Muci- er study, sheep OSE cells examined from the site of nous tumors are cystic tumors with locules lined with stigma formation showed evidence of oxidative DNA mucin-secreting epithelial cells resembling either endo- damage, p53 expression, and apoptosis [17]. cervical or colonic epithelium. They comprise approx- imately 8–10% of primary epithelial ovarian tumors. 3.2. Hypothesis 2 Endometrioid tumors are tumors with epithelial cells resembling endometrial glands of the endometrium and Another hypothesis explaining the relationship be- together with Clear cell lesions constitute about 10% tween ovulation history and ovarian cancer risk in- of epithelial tumors. Other tumor cell types include volves the exposure of HOSE cells to the ovarian stro- Brenner, mixed epithelial type and undifferentiated. ma [18,19] (Fig. 1). Normally, the OSE is separated from the stroma by a basement membrane and a layer of thin connective tissue [11]. The formation of an in- 3. Epidemiology clusion cyst breaks down that barrier and brings HOSE cells into the hormonal milieu of the stroma, prompting Although the etiology of ovarian cancer is unknown, neoplastic growth [20]. scientists have proposed several hypotheses to explain the epidemiologic factors correlating with its incidence. 3.3. Hypothesis 3 Factors that have been associated with a lower risk of ovarian cancer include having had one or more full- The fact that the incidence of ovarian cancer increas- term pregnancies, having used oral contraceptives, hav- es dramatically in women above the age of 45 years ing breast-fed, and having undergone a tubal ligation and peaks between 10 and 20 years after menopause or hysterectomy [5]. All these events would tend to has led tothe development of a “gonadotropin stimu- reduce the number of ovulations a woman has during lation” hypothesis, in which the elevated gonadotropin her lifetime. And although early menarche – which levels found in menopausal and postmenopausal wom- may result in more ovulations – has not been associated en are a causative factor in ovarian cancer [20]. Sup- with an increased incidence of ovarian cancer, studies port this hypothesis are results from several case stud- S.C. Mok et al. / Etiology and pathogenesis of epithelial ovarian cancer 369 Fig. 1. Ovarian microenvironment and the initiation of an epithelial ovarian tumor. We hypothesize that microenvironment in the cortex of the ovary, which has been subjected to chronic inflammation due to either incessant ovulation and/or infection induces dysplatic changes in epithelial cells (including ovarian surface epithelial stem cells) lining the mullerian inclusion cyst. Immune cells infiltration, activated fibroblast formation, and microvessels
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