Hypercholesterolemia induces angiogenesis and accelerates growth of breast tumors in vivo

American Journal of Pathology

Volumn 184, Issue 7, 2014, Pages 2099-2110

  Pelton, Kristine ^a   Coticchia, Christine M ^a   Curatolo, Adam S ^a   Schaffner, Carl P ^b   Zurakowski, David ^a   Solomon, Keith R ^a,c   Moses, Marsha A ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; EZETIMIBE; SATURATED FATTY ACID; AZETIDINE DERIVATIVE; CHOLESTEROL INTAKE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST TUMOR; CAPILLARY DENSITY; CELL PROLIFERATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL INTAKE; CONTROLLED STUDY; FAT INTAKE; FEMALE; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; IN VIVO STUDY; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; POSTMENOPAUSE; PRIORITY JOURNAL; TUMOR GROWTH; ADVERSE EFFECTS; ANIMAL; BLOOD; CANCER TRANSPLANTATION; EXPERIMENTAL MAMMARY NEOPLASM; LIPID DIET; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; AZETIDINES; CELL LINE, TUMOR; CELL PROLIFERATION; CHOLESTEROL; CHOLESTEROL, DIETARY; DIET, HIGH-FAT; FEMALE; HUMANS; HYPERCHOLESTEROLEMIA; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE, SCID; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84903182613     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.03.006     Document Type: Article

References (57)

1. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J Clin 61 2011 69 90
2. H. Shimizu, R.K. Ross, L. Bernstein, R. Yatani, B.E. Henderson, and T.M. Mack Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County Br J Cancer 63 1991 963 966
3. S.A. Bingham, R. Luben, A. Welch, N. Wareham, K.T. Khaw, and N. Day Are imprecise methods obscuring a relation between fat and breast cancer? Lancet 362 2003 212 214
4. A. Emaus, M.B. Veierød, S. Tretli, S.E. Finstad, R. Selmer, A.S. Furberg, L. Bernstein, E. Schlichting, and I. Thune Metabolic profile, physical activity, and mortality in breast cancer patients Breast Cancer Res Treat 121 2010 651 660
5. W.K. Owiredu, S. Donkor, B.W. Addai, and N. Amidu Serum lipid profile of breast cancer patients Pak J Biol Sci 12 2009 332 338
6. A.H. Eliassen, G.A. Colditz, B. Rosner, W.C. Willett, and S.E. Hankinson Adult weight change and risk of postmenopausal breast cancer JAMA 296 2006 193 201
7. K. Simons, and E. Ikonen How cells handle cholesterol Science 290 2000 1721 1726
8. R.E. Soccio, and J.L. Breslow Intracellular cholesterol transport Arterioscler Thromb Vasc Biol 24 2004 1150 1160
9. C. Danilo, and P.G. Frank Cholesterol and breast cancer development Curr Opin Pharmacol 12 2012 677 682
10. J.A. Kaye, C.R. Meier, A.M. Walker, and H. Jick Statin use, hyperlipidaemia, and the risk of breast cancer Br J Cancer 86 2002 1436 1439
11. J.P. Desager, and Y. Horsmans Clinical pharmacokinetics of 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors Clin Pharmacokinet 31 1996 348 371
12. D.M. Boudreau, J.S. Gardner, K.E. Malone, S.R. Heckbert, D.K. Blough, and J.R. Daling The association between 3-hydroxy-3-methylglutaryl coenzyme A inhibitor use and breast carcinoma risk among postmenopausal women: A case-control study Cancer 100 2004 2308 2316
13. J.A. Cauley, A. McTiernan, R.J. Rodabough, A. LaCroix, D.C. Bauer, K.L. Margolis, E.D. Paskett, M.Z. Vitolins, C.D. Furberg, R.T. Chlebowski Women's Health Initiative Research Group Statin use and breast cancer: prospective results from the Women's Health Initiative J Natl Cancer Inst 98 2006 700 707
14. G. Fagherazzi, A. Fabre, M.C. Boutron-Ruault, and F. Clavel-Chapelon Serum cholesterol level, use of a cholesterol-lowering drug, and breast cancer: results from the prospective E3N cohort Eur J Cancer Prev 19 2010 120 125
15. J.A. Cauley, J.M. Zmuda, L.Y. Lui, T.A. Hillier, R.B. Ness, K.L. Stone, S.R. Cummings, and D.C. Bauer Lipid-lowering drug use and breast cancer in older women: A prospective study J Womens Health (Larchmt) 12 2003 749 756
16. A.S. Kumar, C.C. Benz, V. Shim, C.A. Minami, D.H. Moore, and L.J. Esserman Estrogen receptor-negative breast cancer is less likely to arise among lipophilic statin users Cancer Epidemiol Biomarkers Prev 17 2008 1028 1033
17. E.J. Jacobs, C.C. Newton, M.J. Thun, and S.M. Gapstur Long-term use of cholesterol-lowering drugs and cancer incidence in a large United States cohort Cancer Res 71 2011 1763 1771
18. C.M. Kitahara, A. Berrington de González, N.D. Freedman, R. Huxley, Y. Mok, S.H. Jee, and J.M. Samet Total cholesterol and cancer risk in a large prospective study in Korea J Clin Oncol 29 2011 1592 1598
19. T.P. Ahern, L. Pedersen, M. Tarp, D.P. Cronin-Fenton, J.P. Garne, R.A. Silliman, H.T. Sørensen, and T.L. Lash Statin prescriptions and breast cancer recurrence risk: A Danish nationwide prospective cohort study J Natl Cancer Inst 103 2011 1461 1468
20. Y.K. Chae, M.E. Valsecchi, J. Kim, A.L. Bianchi, D. Khemasuwan, A. Desai, and W. Tester Reduced risk of breast cancer recurrence in patients using ACE inhibitors, ARBs, and/or statins Cancer Invest 29 2011 585 593
21. M.L. Kwan, L.A. Habel, E.D. Flick, C.P. Quesenberry, and B. Caan Post-diagnosis statin use and breast cancer recurrence in a prospective cohort study of early stage breast cancer survivors Breast Cancer Res Treat 109 2008 573 579
22. K.R. Solomon, and M.R. Freeman Do the cholesterol-lowering properties of statins affect cancer risk? Trends Endocrinol Metab 19 2008 113 121
23. K.R. Solomon, K. Pelton, K. Boucher, J. Joo, C. Tully, D. Zurakowski, C.P. Schaffner, J. Kim, and M.R. Freeman Ezetimibe is an inhibitor of tumor angiogenesis Am J Pathol 174 2009 1017 1026
24. L. Zhuang, J. Kim, R.M. Adam, K.R. Solomon, and M.R. Freeman Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts J Clin Invest 115 2005 959 968
25. E.A. Mostaghel, K.R. Solomon, K. Pelton, M.R. Freeman, and R.B. Montgomery Impact of circulating cholesterol levels on growth and intratumoral androgen concentration of prostate tumors PLoS One 7 2012 e30062
26. G. Llaverias, C. Danilo, I. Mercier, K. Daumer, F. Capozza, T.M. Williams, F. Sotgia, M.P. Lisanti, and P.G. Frank Role of cholesterol in the development and progression of breast cancer Am J Pathol 178 2011 402 412
27. N. Alikhani, R.D. Ferguson, R. Novosyadlyy, E.J. Gallagher, E.J. Scheinman, S. Yakar, and D. LeRoith Mammary tumor growth and pulmonary metastasis are enhanced in a hyperlipidemic mouse model Oncogene 32 2013 961 967
28. J. Yang, D.R. Bielenberg, S.J. Rodig, R. Doiron, M.C. Clifton, A.L. Kung, R.K. Strong, D. Zurakowski, and M.A. Moses Lipocalin 2 promotes breast cancer progression Proc Natl Acad Sci U S A 106 2009 3913 3918
29. R. Roy, S. Rodig, D. Bielenberg, D. Zurakowski, and M.A. Moses ADAM12 transmembrane and secreted isoforms promote breast tumor growth: A distinct role for ADAM12-S protein in tumor metastasis J Biol Chem 286 2011 20758 20768
30. K. Boucher, C.S. Siegel, P. Sharma, P.V. Hauschka, and K.R. Solomon HMG-CoA reductase inhibitors induce apoptosis in pericytes Microvasc Res 71 2006 91 102
31. D.R. Bielenberg, Y. Hida, A. Shimizu, A. Kaipainen, M. Kreuter, C.C. Kim, and M. Klagsbrun Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype J Clin Invest 114 2004 1260 1271
32. A. Endo, Y. Tsujita, M. Kuroda, and K. Tanzawa Effects of ML-236B on cholesterol metabolism in mice and rats: lack of hypocholesterolemic activity in normal animals Biochim Biophys Acta 575 1979 266 276
33. J.M. Dietschy, and S.D. Turley Control of cholesterol turnover in the mouse J Biol Chem 277 2002 3801 3804
34. A. Endo Chemistry, biochemistry, and pharmacology of HMG-CoA reductase inhibitors Klin Wochenschr 66 1988 421 427
35. W. Tang, Y. Ma, and L. Yu Plasma cholesterol is hyperresponsive to statin in ABCG5/ABCG8 transgenic mice Hepatology 44 2006 1259 1266
36. S.W. Altmann, H.R. Davis Jr., L.J. Zhu, X. Yao, L.M. Hoos, G. Tetzloff, S.P. Iyer, M. Maguire, A. Golovko, M. Zeng, L. Wang, N. Murgolo, and M.P. Graziano Niemann-Pick C1 like 1 protein is critical for intestinal cholesterol absorption Science 303 2004 1201 1204
37. H.R. Davis Jr., L.J. Zhu, L.M. Hoos, G. Tetzloff, M. Maguire, J. Liu, X. Yao, S.P. Iyer, M.H. Lam, E.G. Lund, P.A. Detmers, M.P. Graziano, and S.W. Altmann Niemann-Pick C1 like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis J Biol Chem 279 2004 33586 33592
38. R.H. Knopp, H. Gitter, T. Truitt, H. Bays, C.V. Manion, L.J. Lipka, A.P. LeBeaut, R. Suresh, B. Yang, E.P. Veltri Ezetimibe Study Group Effects of ezetimibe, a new cholesterol absorption inhibitor, on plasma lipids in patients with primary hypercholesterolemia Eur Heart J 24 2003 729 741
39. L. Jia, J.L. Betters, and L. Yu Niemann-pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport Annu Rev Physiol 73 2011 239 259
40. A.H. Lichtman, S.K. Clinton, K. Iiyama, P.W. Connelly, P. Libby, and M.I. Cybulsky Hyperlipidemia and atherosclerotic lesion development in LDL receptor-deficient mice fed defined semipurified diets with and without cholate Arterioscler Thromb Vasc Biol 19 1999 1938 1944
41. F. Parhami, Y. Tintut, W.G. Beamer, N. Gharavi, W. Goodman, and L.L. Demer Atherogenic high-fat diet reduces bone mineralization in mice J Bone Miner Res 16 2001 182 188
42. S.J. Freedland, J. Mavropoulos, A. Wang, M. Darshan, W. Demark-Wahnefried, W.J. Aronson, P. Cohen, D. Hwang, B. Peterson, T. Fields, S.V. Pizzo, and W.B. Isaacs Carbohydrate restriction, prostate cancer growth, and the insulin-like growth factor axis Prostate 68 2008 11 19
43. C.A. Fernandez, L. Yan, G. Louis, J. Yang, J.L. Kutok, and M.A. Moses The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients Clin Cancer Res 11 2005 5390 5395
44. C.A. Fernandez, R. Roy, S. Lee, J. Yang, D. Panigrahy, K.J. Van Vliet, and M.A. Moses The anti-angiogenic peptide, loop 6, binds insulin-like growth factor-1 receptor J Biol Chem 285 2010 41886 41895
45. G. Bergers, and S. Song The role of pericytes in blood-vessel formation and maintenance Neuro Oncol 7 2005 452 464
46. C.P. Schaffner Prostatic cholesterol metabolism: regulation and alteration Prog Clin Biol Res 75A 1981 279 324
47. M.J. Hoffer, M.M. van Eck, F. Petrij, A. van der Zee, E. de Wit, D. Meijer, G. Grosveld, L.M. Havekes, M.H. Hofker, and R.R. Frants The mouse low density lipoprotein receptor gene: cDNA sequence and exon-intron structure Biochem Biophys Res Commun 191 1993 880 886
48. M. Masquelier, S. Vitols, and C. Peterson Low-density lipoprotein as a carrier of antitumoral drugs: in vivo fate of drug-human low-density lipoprotein complexes in mice Cancer Res 46 1986 3842 3847
49. S.G. Young, J.L. Witztum, D.C. Casal, L.K. Curtiss, and S. Bernstein Conservation of the low density lipoprotein receptor-binding domain of apoprotein B: demonstration by a new monoclonal antibody, MB47 Arteriosclerosis 6 1986 178 188
50. J.M. Walsh, and M. Pignone Drug treatment of hyperlipidemia in women JAMA 291 2004 2243 2252
51. E.D. Flick, L.A. Habel, K.A. Chan, S.K. Van Den Eeden, V.P. Quinn, R. Haque, E.J. Orav, J.D. Seeger, M.C. Sadler, C.P. Quesenberry Jr., B. Sternfeld, S.J. Jacobsen, R.A. Whitmer, and B.J. Caan Statin use and risk of prostate cancer in the California Men's Health Study Cohort Cancer Epidemiol Biomarkers Prev 16 2007 2218 2225
52. E.A. Platz, M.F. Leitzmann, K. Visvanathan, E.B. Rimm, M.J. Stampfer, W.C. Willett, and E. Giovannucci Statin drugs and risk of advanced prostate cancer J Natl Cancer Inst 98 2006 1819 1825
53. US Department of Health and Human Services. Health, United States, 2010: with special feature on death and dying. Hyattsville (MD): National Center for Health Statistics (US). DHHS Pub No. 2011-1232. Available from: US Government Printing Office, Washington, DC; 76-641496
54. L.J. McGhan, A.E. McCullough, C.A. Protheroe, A.C. Dueck, J.J. Lee, R. Nunez-Nateras, E.P. Castle, R.J. Gray, N. Wasif, M.P. Goetz, J.R. Hawse, T.J. Henry, M.T. Barrett, H.E. Cunliffe, and B.A. Pockaj Androgen receptor-positive triple negative breast cancer: A unique breast cancer subtype Ann Surg Oncol 21 2014 361 367
55. E.R. Nelson, S.E. Wardell, J.S. Jasper, S. Park, S. Suchindran, M.K. Howe, N.J. Carver, R.V. Pillai, P.M. Sullivan, V. Sondhi, M. Umetani, J. Geradts, and D.P. McDonnell 27-Hydroxycholesterol links hypercholesterolemia and breast cancer pathophysiology Science 342 2013 1094 1098
56. H. Wu, R.M. Gower, H. Wang, X.Y. Perrard, R. Ma, D.C. Bullard, A.R. Burns, A. Paul, C.W. Smith, S.I. Simon, and C.M. Ballantyne Functional role of CD11c+ monocytes in atherogenesis associated with hypercholesterolemia Circulation 119 2009 2708 2717
57. R.D. Leek, C.E. Lewis, R. Whitehouse, M. Greenall, J. Clarke, and A.L. Harris Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma Cancer Res 56 1996 4625 4629