Obesity contributes to ovarian cancer metastatic success through increased lipogenesis, enhanced vascularity, and decreased infiltration of M1 macrophages

Cancer Research

Volumn 75, Issue 23, 2015, Pages 5046-5057

  Liu, Yueying ^a   Metzinger, Matthew N ^a   Lewellen, Kyle A ^a   Cripps, Stephanie N ^b   Carey, Kyle D ^a   Harper, Elizabeth I ^c   Shi, Zonggao ^a   Tarwater, Laura ^a   Grisoli, Annie ^a   Lee, Eric ^a   Slusarz, Ania ^d   Yang, Jing ^a   Loughran, Elizabeth A ^a   Conley, Kaitlyn ^a   Johnson, Jeff J ^a   Klymenko, Yuliya ^a   Bruney, Lana ^a,d   Liang, Zhong ^a   Dovichi, Norman J ^a   Cheatham, Bentley ^e   Leevy, W Matthew ^a   Stack, M Sharon ^a   more..

^a UNIVERSITY OF NOTRE DAME   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

^c EARLHAM COLLEGE   (United States)

^d University of Missouri   (United States)

^e Zen Bio Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL ADHESION; CELL INFILTRATION; CONTROLLED STUDY; DIET INDUCED OBESITY; EX VIVO STUDY; EXPLANT; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPOGENESIS; MACROPHAGE; MESOTHELIUM CELL; MOUSE; NONHUMAN; OBESITY; OVARY CARCINOMA; PRIORITY JOURNAL; TUMOR VASCULARIZATION; TUMOR VOLUME; WESTERN DIET; ANIMAL; IMMUNOLOGY; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION; VASCULARIZATION; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; FEMALE; HETEROGRAFTS; HUMANS; LIPOGENESIS; MACROPHAGES; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; OBESITY; OVARIAN NEOPLASMS;

EID: 84955321442     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0706     Document Type: Article

References (50)

1. U.S. Cancer Statistics Working Group. United States Cancer Statistics: 1999-2011 Incidence and Mortality Web Based Report. Bethesda, MD: Department of Health and Human Services, Centers for Disease Control and Prevention, and National Cancer Institute; 2014.
2. Cramer DW. The epidemiology of endometrial and ovarian cancer. Hematol Oncol Clin North Am 2012; 26: 1-12.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
4. Siegel R, Naishadham D, Jemal A. Cancer statistics 2013. CA Cancer J Clin 2013; 63: 11-30.
5. American Cancer Society. Cancer facts and figures. Atlanta, GA: American Cancer Society; 2013.
6. Naora H, Montell DJ. Ovarian cancer metastasis: Integrating insights from disparate model organisms. Nat Rev Can 2005; 5: 355-66.
7. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults 1999-2010. JAMA 2012; 307: 491-7.
8. Lahmann PH, Cust AE, Friedenreich CM, Schulz M, Lukanova A, Kaaks R, et al. Anthropometric measures and epithelial ovarian cancer risk in the European Prospective Investigation into Cancer and Nutrition. Int J Cancer 2010; 126: 2404-15.
9. Delort L, Kwiatkowski F, Chalabi N, Satih S, Bignon YJ, Bernard-Gallon DJ. Central adiposity as a major risk factor of ovarian cancer. Anticancer Res 2009; 29: 5229-34.
10. Chionh F, Baglietto L, Krishnan K, English DR, MacInnis RJ, Gertig DM, et al. Physical activity, body size and composition, and overall risk of ovarian cancer. Cancer Causes Control 2010; 21: 2183-94.
11. Yang HP, Trabert B, Murphy MA, Sherman ME, Sampson JN, Brinton LA, et al. Ovarian cancer risk factors by histologic subtypes in the NIH-AARP Diet and Health Study. Int J Cancer 2012; 131: 938-48.
12. Collaborative Group on Epidemiological Studies of Ovarian Cancer. Ovarian cancer and body size: Individual participantmeta-analysis including 25,157 women with ovarian cancer from 47 epidemiological studies. PLoS Med 2012; 9: E1001200.
13. Olsen CM, Nagle CM, Whiteman DC, Ness R, Pearce CL, Pike MC, et al. Obesity and risk of ovarian cancer subtypes: Evidence from the Ovarian Cancer Association Consortium. Endocr Relat Cancer 2013; 20: 251-62.
14. Calle EE, Kaaks R. Overweight, obesity and cancer: Epidemiological evidence and proposed mechanisms. Nat Rev Cancer 2004; 4: 579-91.
15. Protani MM, Nagle CM, Webb PM. Obesity and ovarian cancer survival: A systematic review and meta-analysis. Cancer Prev Res 2012; 5: 901-10.
16. Schildkraut JM, Alberg AJ, Bandera EV, Barnholtz-Sloan J, Bondy M, Cote MJ, et al. A multi-center population-based case-control study of ovarian cancer in African-American women: The African American Cancer Epidemiology Study (AACES). BMC Cancer 2014; 14: 688-92
17. Bae HS, Kim HJ, Hong JH, Lee JK, Lee NW, Song JY. Obesity and epithelial ovarian cancer survival: A systematic review and meta-analysis. J Ovarian Res 2014; 7: 41.
18. Yang HS, Yoon C, Myung SK, Park SM. Effoct of obesity on survival of women with epithelial ovarian cancer: A systematic review and metaanalysis of observationsl studies. Int J Gynecol Cancer 2011; 21: 1525-32.
19. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol 2010; 177: 1053-64.
20. Niedbala MJ,Crickard K, Bernacki RJ. Interactions of human ovarian tumor cells with humanmesothelial cells grown on extracellular matrix. An in vitro model system for studying tumor cell adhesion and invasion. Exp Cell Res 1985; 160: 499-513.
21. Barbolina MV, Moss NM, Westfall SD, Liu Y, Burkhalter RJ, Marga F, et al. Microenvironmental regulation of ovarian cancer metastasis. Cancer Treat Res 2009; 149: 319-34
22. Tebbe C, Chhina J, Dar SA, Sarigiannis K, Giri S, Munkarah AR, et al. Metformin limits the adipocyte tumor-promoting effect on ovarian cancer. Oncotarget 2014; 5: 4746-64.
23. Krist LF, Kerremans M, Broekhuis-Fluitsma DM, Eestermans IL, Meyer S, Beelen RH. Milky spots in the greater omentum are predominant sites of local tumour cell proliferation and accumulation in the peritoneal cavity. Cancer Immunol Immunother 1998; 47: 205-12.
24. Clark R, Krishnan V, Schoof M, Rodriguez I, Theriault B, Chekmareva M, et al. Milky spots promote ovarian cancer metastatic colonization of peritoneal adipose in experimental models. Am J Pathol 2013; 183: 576-91.
25. Hagiwara A, Takahashi T, Sawai K, Taniguchi H, Shimotsuma M, Okano S, et al. Milky spots as the implantation site for malignant cells in peritoneal dissemination in mice. Can Res 1993; 53: 687-92.
26. Gerber SA, Rybalko VY, Bigelow CE, Lugade AA, Foster TH, Frelinger JG, et al. Preferential attachment of peritoneal tumor metastases to omental immune aggregates and possible role of a unique vascular microenvironment in metastatic survival and growth. Am J Path 2006; 169: 1739-52.
27. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt MR, et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 2011; 11: 1498-503.
28. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, et al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 2000; 21: 585-91.
29. Brown MV, Compton SA, Milburn MV, Lawton KA, Cheatham B. Metabolomic signatures in lipid-loaded HepaRGs reveal pathways involved in steatotic progression. Obesity 2013; 21: E561-70.
30. Kenny HA, Dogan S, Zillhardt M, K Mitra A, Yamada SD, Krausz T, et al. Organotypic models of metastasis: A three-dimensional culture mimicking the human peritoneum and omentum for the study of the early steps of ovarian cancer metastasis. Cancer Treat Res 2009; 149: 335-51.
31. Lengyel E, Burdette JE, Kenny HA, Matei D, Pilrose J, Haluska P, et al. Epithelial ovarian cancer experimental models. Oncogene 2014; 33: 3619-33.
32. Bruney L, Conley KC, Moss NM, Liu Y, Stack MS. Membrane-type I matrix metalloproteinase-dependent ectodomain shedding of mucin16/CA-125 on ovarian cancer cells modulates adhesion and invasion of peritoneal mesothelium. Biol Chem 2014; 395: 1221-31.
33. Lewellen K, Metzinger MN, Liu Y, Stack MS. Quantitation of intra-peritoneal ovarian cancer metastasis. J Vis Exp 2015. In press.
34. Nilsson C, Raun K, Yan F, Larsen MO, Tang-Christensen M. Laboratory animals as surrogate models of human obesity. Acta Pharmacologica Sinica 2012; 33: 173-81.
35. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its huma homologue. Nature 1994; 372: 425-31.
36. Makowski L, Zhou C, Zhong Y, Kuan PF, Fan C, Sampey BP, et al. Obesity increases tumor aggressiveness in a genetically engineered mouse model of serous ovarian cancer. Gyn Oncol 2014; 133: 90-7.
37. Guo D, Bell EH, Mischel P, Chakravarti A. Targeting SREBP1-driven lipid metabolism to treat cancer. Curr Pharm Des 2014; 20: 2619-26.
38. Park J, Morley TS, Kim M, Clegg DJ, Scherer PE. Obesity and cancer - mechanisms underlying tumour progression and recurrence. Nat Rev Endocrinol 2014; 10: 455-65.
39. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-74.
40. Colvin EK. Tumor-associated macrophages contribute to tumor progression in ovarian cancer. Front Oncol 2014; 4: Article 137.
41. Brown MS, Goldstein JL. The SREBP pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcriptions factor. Cell 1997; 89: 331-40.
42. Hawkins JL, Robbins MD, Warren LC, Xia D, Petras SF, Valentine JJ, et al. Pharmacologic inhibition of site 1 protease activity inhibits sterol regulatory element-binding protein processing and reduces lipogenic enzyme gene expression and lipid synthesis in cultured cells and experimental animals. J Pharmacol Exp Ther 2008; 326: 801-8.
43. Slaughter KN, Thai T, Penaroza S, Benbrook DM, Thavathiru E, Ding K, et al. Measurements of adiposity as clinical biomarkers for first-line bevacizumab-based chemotherapy in epithelial ovarian cancer. Gynecol Oncol 2014; 133: 11-5.
44. Yang C, Lee H, Pal S, Jove V, Deng J, Zhang W, et al. B cells promote tumor progression via STAT3 regulated angiogenesis. PLoS One 2013; 5: E64159.
45. Yang C, Lee H, Jove V, Deng J, Zhang W, Liu X, et al. Prognostic significance of B cells and pSTAT3 in patients with ovarian cancer. PLoS One 2013; 8: E54029.
46. Naora H. Heterotypic cellular interactions in the ovarian tumor microenvironment: Biological significance and therapeutic implications. Front Oncol 2014; 4: Article 18.
47. Zhang M, He Y, Sun X, Li Z, Wang W, Zhao A, et al. A high M1/M2 ratio of tumor-associated macrophages is associated with extended survival in ovarian cancer patients. J Ovarian Res 2014; 7: 1-16.
48. Grecius G,Westerberg L, Davey EJ, Buentke E, Scheynius A, Thyberg J, et al. Microvilli structures on B lymphocytes: Inducible functional domains? Int Immunol 2004; 16: 353-64.
49. Murai T, Sato M, Nishiyama H, Suga M, Sato C. Ultrastructural analysis of nanogold-labeled cell surface microvilli in liquid by atmospheric scanning electron microscopy and their relevance in cell adhesion. Int J Mol Sci 2013; 14: 20809-19.
50. Lomakina EB, Marsh G, Waugh RE. Cell surface topography is a regulator of molecular interactions during chemokine-induced neutrophil spreading. Biophys J 2014; 107: 1302-12.