期刊论文详细信息
Journal of Hematology & Oncology
Ovarian serous carcinoma: recent concepts on its origin and carcinogenesis
Wenxin Zheng1  Beihua Kong2  Li Xiang2  Oluwole Fadare3  Jie Li2 
[1] Department of Pathology, University of Arizona, 1501 N. Campbell Avenue, #5224A, Tucson, AZ 85724, USA;Department of Pathology, University of Arizona College of Medicine, Tucson, AZ, USA;Department of Pathology, Microbiology and Immunology, Vanderbilt University School of Medicine, Nashville, TN, USA
关键词: p53 signatures;    Serous carcinoma;    Carcinogenesis;    Fallopian tube;    Ovarian cancer;   
Others  :  822559
DOI  :  10.1186/1756-8722-5-8
 received in 2012-02-20, accepted in 2012-03-09,  发布年份 2012
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【 摘 要 】

Recent morphologic and molecular genetic studies have led to a paradigm shift in our conceptualization of the carcinogenesis and histogenesis of pelvic (non-uterine) serous carcinomas. It appears that both low-grade and high-grade pelvic serous carcinomas that have traditionally been classified as ovarian in origin, actually originate, at least in a significant subset, from the distal fallopian tube. Clonal expansions of the tubal secretory cell probably give rise to serous carcinomas, and the degree of ciliated conversion is a function of the degree to which the genetic hits deregulate normal differentiation. In this article, the authors review the evidentiary basis for aforementioned paradigm shift, as well as its potential clinical implications.

【 授权许可】

   
2012 Li et al; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin 2011, 61:69-90.
  • [2]Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ: Cancer statistics, 2008. CA Cancer J Clin 2008, 58:71-96.
  • [3]Partridge EE, Barnes MN: Epithelial ovarian cancer: prevention, diagnosis, and treatment. CA Cancer J Clin 1999, 49:297-320.
  • [4]Ries LA, Melbert D, Krapcho M, et al (Eds): SEER cancer statistics review, 1975-2004 Bethesda, Md.: National Cancer Institute; 2007.
  • [5]Seidman JD, Horkayne-Szakaly I, Haiba M, Boice CR, Kurman RJ, Ronnett BM: The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin. Int J Gynecol Pathol 2004, 23:41-44.
  • [6]Selvaggi SM: Tumors of the ovary, maldeveloped gonads, fallopian tube, and broad ligament. Arch Pathol Lab Med 2000, 124:477.
  • [7]Colgan TJ, Murphy J, Cole DE, Narod S, Rosen B: Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status. Am J Surg Pathol 2001, 25:1283-1289.
  • [8]Powell CB, Kenley E, Chen LM, Crawford B, McLennan J, Zaloudek C, Komaromy M, Beattie M, Ziegler J: Risk-reducing salpingo-oophorectomy in BRCA mutation carriers: role of serial sectioning in the detection of occult malignancy. J Clin Oncol 2005, 23:127-132.
  • [9]Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP: The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 2006, 30:230-236.
  • [10]Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, et al.: A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 2007, 211:26-35.
  • [11]Mehrad M, Ning G, Chen EY, Mehra KK, Crum CP: A pathologist's road map to benign, precancerous, and malignant intraepithelial proliferations in the fallopian tube. Adv Anat Pathol 2010, 17:293-302.
  • [12]Kurman RJ, Shih Ie M: Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 2011, 42:918-931.
  • [13]Ho CL, Kurman RJ, Dehari R, Wang TL, Shih Ie M: Mutations of BRAF and KRAS precede the development of ovarian serous borderline tumors. Cancer Res 2004, 64:6915-6918.
  • [14]Korner M, Burckhardt E, Mazzucchelli L: Different proportions of aneusomic cells in ovarian inclusion cysts associated with serous borderline tumours and serous high-grade carcinomas support different pathogenetic pathways. J Pathol 2005, 207:20-26.
  • [15]Malpica A, Deavers MT, Lu K, Bodurka DC, Atkinson EN, Gershenson DM, Silva EG: Grading ovarian serous carcinoma using a two-tier system. Am J Surg Pathol 2004, 28:496-504.
  • [16]Fleming JS, Beaugie CR, Haviv I, Chenevix-Trench G, Tan OL: Incessant ovulation, inflammation and epithelial ovarian carcinogenesis: revisiting old hypotheses. Mol Cell Endocrinol 2006, 247:4-21.
  • [17]Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC: Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001, 22:255-288.
  • [18]Cheng W, Liu J, Yoshida H, Rosen D, Naora H: Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract. Nat Med 2005, 11:531-537.
  • [19]Naora H: Developmental patterning in the wrong context: the paradox of epithelial ovarian cancers. Cell Cycle 2005, 4:1033-1035.
  • [20]Bowen NJ, Logani S, Dickerson EB, Kapa LB, Akhtar M, Benigno BB, McDonald JF: Emerging roles for PAX8 in ovarian cancer and endosalpingeal development. Gynecol Oncol 2007, 104:331-337.
  • [21]Bhuyan P, Mahapatra S, Sethy S, Parida P, Satpathy S: Extraovarian primary peritoneal papillary serous carcinoma. Arch Gynecol Obstet 2010, 281:561-564.
  • [22]August CZ, Murad TM, Newton M: Multiple focal extraovarian serous carcinoma. Int J Gynecol Pathol 1985, 4:11-23.
  • [23]Dalrymple JC, Bannatyne P, Russell P, Solomon HJ, Tattersall MH, Atkinson K, Carter J, Duval P, Elliott P, Friedlander M, et al.: Extraovarian peritoneal serous papillary carcinoma. A clinicopathologic study of 31 cases. Cancer 1989, 64:110-115.
  • [24]Lauchlan SC: The secondary Mullerian system. Obstet Gynecol Surv 1972, 27:133-146.
  • [25]Zheng W, Li N, Wang J, Ulukus EC, Ulukus M, Arici A, Liang SX: Initial endometriosis showing direct morphologic evidence of metaplasia in the pathogenesis of ovarian endometriosis. Int J Gynecol Pathol 2005, 24:164-172.
  • [26]Crum CP, Drapkin R, Kindelberger D, Medeiros F, Miron A, Lee Y: Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin Med Res 2007, 5:35-44.
  • [27]Levanon K, Crum C, Drapkin R: New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J Clin Oncol 2008, 26:5284-5293.
  • [28]Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, et al.: Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am J Surg Pathol 2007, 31:161-169.
  • [29]Carlson JW, Miron A, Jarboe EA, Parast MM, Hirsch MS, Lee Y, Muto MG, Kindelberger D, Crum CP: Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention. J Clin Oncol 2008, 26:4160-4165.
  • [30]Crum CP: Intercepting pelvic cancer in the distal fallopian tube: theories and realities. Mol Oncol 2009, 3:165-170.
  • [31]Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P, Verheijen RH: Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 2001, 195:451-456.
  • [32]Finch A, Shaw P, Rosen B, Murphy J, Narod SA, Colgan TJ: Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol 2006, 100:58-64.
  • [33]Leeper K, Garcia R, Swisher E, Goff B, Greer B, Paley P: Pathologic findings in prophylactic oophorectomy specimens in high-risk women. Gynecol Oncol 2002, 87:52-56.
  • [34]Lamb JD, Garcia RL, Goff BA, Paley PJ, Swisher EM: Predictors of occult neoplasia in women undergoing risk-reducing salpingo-oophorectomy. Am J Obstet Gynecol 2006, 194:1702-1709.
  • [35]Olivier RI, van Beurden M, Lubsen MA, Rookus MA, Mooij TM, van de Vijver MJ, van't Veer LJ: Clinical outcome of prophylactic oophorectomy in BRCA1/BRCA2 mutation carriers and events during follow-up. Br J Cancer 2004, 90:1492-1497.
  • [36]Callahan MJ, Crum CP, Medeiros F, Kindelberger DW, Elvin JA, Garber JE, Feltmate CM, Berkowitz RS, Muto MG: Primary fallopian tube malignancies in BRCA-positive women undergoing surgery for ovarian cancer risk reduction. J Clin Oncol 2007, 25:3985-3990.
  • [37]Hermsen BB, van Diest PJ, Berkhof J, Menko FH, Gille JJ, Piek JM, Meijer S, Winters HA, Kenemans P, Mensdorff-Pouilly S, Verheijen RH: Low prevalence of (pre) malignant lesions in the breast and high prevalence in the ovary and Fallopian tube in women at hereditary high risk of breast and ovarian cancer. Int J Cancer 2006, 119:1412-1418.
  • [38]Finch A, Beiner M, Lubinski J, Lynch HT, Moller P, Rosen B, Murphy J, Ghadirian P, Friedman E, Foulkes WD, et al.: Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation. JAMA 2006, 296:185-192.
  • [39]Salvador S, Rempel A, Soslow RA, Gilks B, Huntsman D, Miller D: Chromosomal instability in fallopian tube precursor lesions of serous carcinoma and frequent monoclonality of synchronous ovarian and fallopian tube mucosal serous carcinoma. Gynecol Oncol 2008, 110:408-417.
  • [40]Przybycin CG, Kurman RJ, Ronnett BM, Shih Ie M, Vang R: Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am J Surg Pathol 2010, 34:1407-1416.
  • [41]Boyd C, McCluggage WG: Low-grade ovarian serous neoplasms (Low-Grade Serous Carcinoma and Serous Borderline Tumor) associated with high-grade serous carcinoma or undifferentiated carcinoma: report of a series of cases of an unusual phenomenon. Am J Surg Pathol 2012, 36:368-375.
  • [42]Dehari R, Kurman RJ, Logani S, Shih Ie M: The development of high-grade serous carcinoma from atypical proliferative (borderline) serous tumors and low-grade micropapillary serous carcinoma: a morphologic and molecular genetic analysis. Am J Surg Pathol 2007, 31:1007-1012.
  • [43]Kurman RJ, Shih Ie M: The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 2010, 34:433-443.
  • [44]Piek JM, van Diest PJ, Zweemer RP, Kenemans P, Verheijen RH: Tubal ligation and risk of ovarian cancer. Lancet 2001, 358:844.
  • [45]Levanon K, Ng V, Piao HY, Zhang Y, Chang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, Drapkin R: Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 2010, 29:1103-1113.
  • [46]Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, Bogomolniy F, Olvera N, Lin O, Soslow RA, et al.: Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS One 2010, 5:e10358.
  • [47]Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S, Crum CP: A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecol Oncol 2008, 109:168-173.
  • [48]Quick CM, Ning G, Bijron J, Laury A, Wei TS, Chen EY, Vargas SO, Betensky RA, McKeon FD, Xian W, Crum CP: PAX2-null secretory cell outgrowths in the oviduct and their relationship to pelvic serous cancer. Mod Pathol 2011, 25:455.
  • [49]Chen EY, Mehra K, Mehrad M, Ning G, Miron A, Mutter GL, Monte N, Quade BJ, McKeon FD, Yassin Y, et al.: Secretory cell outgrowth, PAX2 and serous carcinogenesis in the Fallopian tube. J Pathol 2010, 222:110-116.
  • [50]Salani R, Kurman RJ, Giuntoli R, Gardner G, Bristow R, Wang TL, Shih IM: Assessment of TP53 mutation using purified tissue samples of ovarian serous carcinomas reveals a higher mutation rate than previously reported and does not correlate with drug resistance. Int J Gynecol Cancer 2008, 18:487-491.
  • [51]Senturk E, Cohen S, Dottino PR, Martignetti JA: A critical re-appraisal of BRCA1 methylation studies in ovarian cancer. Gynecol Oncol 2010, 119:376-383.
  • [52]Tone AA, Begley H, Sharma M, Murphy J, Rosen B, Brown TJ, Shaw PA: Gene expression profiles of luteal phase fallopian tube epithelium from BRCA mutation carriers resemble high-grade serous carcinoma. Clin Cancer Res 2008, 14:4067-4078.
  • [53]Marquez RT, Baggerly KA, Patterson AP, Liu J, Broaddus R, Frumovitz M, Atkinson EN, Smith DI, Hartmann L, Fishman D, et al.: Patterns of gene expression in different histotypes of epithelial ovarian cancer correlate with those in normal fallopian tube, endometrium, and colon. Clin Cancer Res 2005, 11:6116-6126.
  • [54]Shih Ie M, Kurman RJ: Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 2004, 164:1511-1518.
  • [55]Kurman RJ, ShihIe M: The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 2011, 34:433-443.
  • [56]Li J, Abushahin N, Pang S, Xiang L, Chambers SK, Fadare O, Kong B, Zheng W: Tubal origin of 'ovarian' low-grade serous carcinoma. Mod Pathol 2011, 24:1488-1499.
  • [57]Kurman RJ, Vang R, Junge J, Hannibal CG, Kjaer SK, Shih Ie M: Papillary tubal hyperplasia: the putative precursor of ovarian atypical proliferative (borderline) serous tumors, noninvasive implants, and endosalpingiosis. Am J Surg Pathol 2011, 35:1605-1614.
  • [58]Laury AR, Ning G, Quick CM, Bijron J, Parast MM, Betensky RA, Vargas SO, McKeon FD, Xian W, Nucci MR, Crum CP: Fallopian tube correlates of ovarian serous borderline tumors. Am J Surg Pathol 2011, 35:1759-1765.
  • [59]Scully RE: Pathology of ovarian cancer precursors. J Cell Biochem Suppl 1995, 23:208-218.
  • [60]Smith Sehdev AE, Sehdev PS, Kurman RJ: Noninvasive and invasive micropapillary (low-grade) serous carcinoma of the ovary: a clinicopathologic analysis of 135 cases. Am J Surg Pathol 2003, 27:725-736.
  • [61]Burks RT, Sherman ME, Kurman RJ: Micropapillary serous carcinoma of the ovary. A distinctive low-grade carcinoma related to serous borderline tumors. Am J Surg Pathol 1996, 20:1319-1330.
  • [62]McKenney JK, Balzer BL, Longacre TA: Patterns of stromal invasion in ovarian serous tumors of low malignant potential (borderline tumors): a reevaluation of the concept of stromal microinvasion. Am J Surg Pathol 2006, 30:1209-1221.
  • [63]Seidman JD, Soslow RA, Vang R, Berman JJ, Stoler MH, Sherman ME, Oliva E, Kajdacsy-Balla A, Berman DM, Copeland LJ: Borderline ovarian tumors: diverse contemporary viewpoints on terminology and diagnostic criteria with illustrative images. Hum Pathol 2004, 35:918-933.
  • [64]Bell DA, Longacre TA, Prat J, Kohn EC, Soslow RA, Ellenson LH, Malpica A, Stoler MH, Kurman RJ: Serous borderline (low malignant potential, atypical proliferative) ovarian tumors: workshop perspectives. Hum Pathol 2004, 35:934-948.
  • [65]Longacre TA, McKenney JK, Tazelaar HD, Kempson RL, Hendrickson MR: Ovarian serous tumors of low malignant potential (borderline tumors): outcome-based study of 276 patients with long-term (> or = 5-year) follow-up. Am J Surg Pathol 2005, 29:707-723.
  • [66]Dubeau L: The cell of origin of ovarian epithelial tumours. Lancet Oncol 2008, 9:1191-1197.
  • [67]Nature CGARN: Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
  • [68]Herrington CS, McCluggage WG: The emerging role of the distal Fallopian tube and p53 in pelvic serous carcinogenesis. J Pathol 2010, 220:5-6.
  • [69]Xian W, Miron A, Roh M, Semmel DR, Yassin Y, Garber J, Oliva E, Goodman A, Mehra K, Berkowitz RS, et al.: The Li-Fraumeni syndrome (LFS): a model for the initiation of p53 signatures in the distal Fallopian tube. J Pathol 2010, 220:17-23.
  • [70]Venkitaraman AR: Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 2002, 108:171-182.
  • [71]Risch HA, McLaughlin JR, Cole DE, Rosen B, Bradley L, Fan I, Tang J, Li S, Zhang S, Shaw PA, Narod SA: Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada. J Natl Cancer Inst 2006, 98:1694-1706.
  • [72]Werness BA, Parvatiyar P, Ramus SJ, Whittemore AS, Garlinghouse-Jones K, Oakley-Girvan I, DiCioccio RA, Wiest J, Tsukada Y, Ponder BA, Piver MS: Ovarian carcinoma in situ with germline BRCA1 mutation and loss of heterozygosity at BRCA1 and TP53. J Natl Cancer Inst 2000, 92:1088-1091.
  • [73]Palmieri M, LeiItao M, Baergen R, et al.: Genetic analysis of ovarian carcinoma histogenesis (Abstract). Gynecol Oncol 2001, 80:277.
  • [74]Norquist BM, Garcia RL, Allison KH, Jokinen CH, Kernochan LE, Pizzi CC, Barrow BJ, Goff BA, Swisher EM: The molecular pathogenesis of hereditary ovarian carcinoma: alterations in the tubal epithelium of women with BRCA1 and BRCA2 mutations. Cancer 2010, 116:5261-5271.
  • [75]Singer G, Kurman RJ, Chang HW, Cho SK, Shih Ie M: Diverse tumorigenic pathways in ovarian serous carcinoma. Am J Pathol 2002, 160:1223-1228.
  • [76]Nakayama K, Nakayama N, Jinawath N, Salani R, Kurman RJ, Shih Ie M, Wang TL: Amplicon profiles in ovarian serous carcinomas. Int J Cancer 2007, 120:2613-2617.
  • [77]Kuo KT, Guan B, Feng Y, Mao TL, Chen X, Jinawath N, Wang Y, Kurman RJ, Shih Ie M, Wang TL: Analysis of DNA copy number alterations in ovarian serous tumors identifies new molecular genetic changes in low-grade and high-grade carcinomas. Cancer Res 2009, 69:4036-4042.
  • [78]Singer G, Oldt R, Cohen Y, Wang BG, Sidransky D, Kurman RJ, Shih Ie M: Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst 2003, 95:484-486.
  • [79]Nakayama K, Nakayama N, Kurman RJ, Cope L, Pohl G, Samuels Y, Velculescu VE, Wang TL, Shih Ie M: Sequence mutations and amplification of PIK3CA and AKT2 genes in purified ovarian serous neoplasms. Cancer Biol Ther 2006, 5:779-785.
  • [80]Sieben NL, Macropoulos P, Roemen GM, Kolkman-Uljee SM, Jan Fleuren G, Houmadi R, Diss T, Warren B, Al Adnani M, De Goeij AP, et al.: In ovarian neoplasms, BRAF, but not KRAS, mutations are restricted to low-grade serous tumours. J Pathol 2004, 202:336-340.
  • [81]Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE: Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 2002, 418:934.
  • [82]Staebler A, Heselmeyer-Haddad K, Bell K, Riopel M, Perlman E, Ried T, Kurman RJ: Micropapillary serous carcinoma of the ovary has distinct patterns of chromosomal imbalances by comparative genomic hybridization compared with atypical proliferative serous tumors and serous carcinomas. Hum Pathol 2002, 33:47-59.
  • [83]Alvarez AA, Moore WF, Robboy SJ, Bentley RC, Gumbs C, Futreal PA, Berchuck A: K-ras mutations in Mullerian inclusion cysts associated with serous borderline tumors of the ovary. Gynecol Oncol 2001, 80:201-206.
  • [84]Haas CJ, Diebold J, Hirschmann A, Rohrbach H, Lohrs U: In serous ovarian neoplasms the frequency of Ki-ras mutations correlates with their malignant potential. Virchows Arch 1999, 434:117-120.
  • [85]Mayr D, Hirschmann A, Lohrs U, Diebold J: KRAS and BRAF mutations in ovarian tumors: a comprehensive study of invasive carcinomas, borderline tumors and extraovarian implants. Gynecol Oncol 2006, 103:883-887.
  • [86]Partridge E, Kreimer AR, Greenlee RT, Williams C, Xu JL, Church TR, Kessel B, Johnson CC, Weissfeld JL, Isaacs C, et al.: Results from four rounds of ovarian cancer screening in a randomized trial. Obstet Gynecol 2009, 113:775-782.
  • [87]Liu B, Nash J, Runowicz C, Swede H, Stevens R, Li Z: Ovarian cancer immunotherapy: opportunities, progresses and challenges. J Hematol Oncol 2010, 3:7. BioMed Central Full Text
  • [88]Sezik M, Ozkaya O, Demir F, Sezik HT, Kaya H: Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow. J Obstet Gynaecol Res 2007, 33:863-869.
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