Leptin deficiency suppresses MMTV-Wnt-1 mammary tumor growth in obese mice and abrogates tumor initiating cell survival

Endocrine-Related Cancer

Volumn 18, Issue 4, 2011, Pages 491-503

  Zheng, Qiao ^a   Dunlap, Sarah M ^b   Zhu, Jinling ^a   Downs Kelly, Erinn ^a   Rich, Jeremy ^a   Hursting, Stephen D ^b,c   Berger, Nathan A ^d   Reizes, Ofer ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b Section of Molecular Genetics and Microbiology   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; BETA1 INTEGRIN; CD24 ANTIGEN; CYTOKERATIN 6; INSULIN; LEPTIN; LEPTIN RECEPTOR; PROTEIN KINASE B; WNT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CANCER STEM CELL; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL SURVIVAL; CONTROLLED STUDY; DILUTION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; IN VIVO CULTURE; LEPTIN DEFICIENCY; MOUSE; NONHUMAN; OBESITY; PROTEIN DEFICIENCY; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; CARCINOMA; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; DOWN-REGULATION; FEMALE; LEPTIN; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, INBRED C57BL; MICE, OBESE; MICE, TRANSGENIC; NEOPLASTIC STEM CELLS; OBESITY; RECEPTORS, LEPTIN; WNT1 PROTEIN;

EID: 80052155796     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-11-0102     Document Type: Article

References (55)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ &Clarke MF 2003 Prospective identification of tumorigenic breast cancer cells. PNAS 100 3983-3988. (doi:10.1073/pnas.0530291100)
2. American Cancer Society 2011 Cancer Facts and Figures 2011. Atlanta, GA, USA: American Cancer Society.
3. Baskin ML, Ard J, Franklin F & Allison DB 2005 Prevalence of obesity in the United States. Obesity Reviews 6 5-7. (doi:10.1111/j.1467-789X.2005. 00165.x)
4. Brakenhielm E, Cao R, Gao B, Angelin B, Cannon B, Parini P & Cao Y 2004 Angiogenesis inhibitor, TNP-470, prevents diet-induced and genetic obesity in mice. Circulation Research 94 1579-1588. (doi:10.1161/01. RES.0000132745.76882.70)
5. Brown AM 2001 Wnt signaling in breast cancer: have we come full circle? Breast Cancer Research 3 351-355. (doi:10.1186/bcr321)
6. Calle EE, Rodriguez C, Walker-Thurmond K & Thun MJ 2003 Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. New England Journal of Medicine 348 1625-1638. (doi:10.1056/ NEJMoa021423)
7. Cao L, Liu X, Lin EJ, Wang C, Choi EY, Riban V, Lin B &During MJ 2010 Environmental and genetic activation of a brain-adipocyte BDNF/leptin axis causes cancer remission and inhibition. Cell 142 52-64. (doi:10.1016/j.cell. 2010.05.029)
8. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J et al. 2009 Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Research 69 1302-1313. (doi:10.1158/0008- 5472.CAN-08-2741)
9. Cheang MC, Voduc D, Bajdik C, Leung S, McKinney S, Chia SK, Perou CM & Nielsen TO 2008 Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clinical Cancer Research 14 1368-1376. (doi:10.1158/1078-0432.CCR-07-1658)
10. Chen MS, Woodward WA, Behbod F, Peddibhotla S, Alfaro MP, Buchholz TA & Rosen JM 2007 Wnt/beta-catenin mediates radiation resistance of Sca1 + progenitors in an immortalized mammary gland cell line. Journal of Cell Science 120 468-477. (doi:10.1242/jcs.03348)
11. Cho RW, Wang X, Diehn M, Shedden K, Chen GY, Sherlock G, Gurney A, Lewicki J & Clarke MF 2008 Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells 26 364-371. (doi:10.1634/stemcells.2007-0440)
12. Cleary MP, Phillips FC, Getzin SC, Jacobson TL, Jacobson MK, Christensen TA, Juneja SC, Grande JP & Maihle NJ 2003 Genetically obese MMTV-TGF-alpha/Lep(ob)Lep( ob) female mice do not develop mammary tumors. Breast Cancer Research and Treatment 77 205-215. (doi:10.1023/A:1021891825399)
13. Cleary MP, Juneja SC, Phillips FC, Hu X, Grande JP &Maihle NJ 2004 Leptin receptor-deficient MMTV-TGF-alpha/Lepr(db)Lepr(db) female mice do not develop oncogene-induced mammary tumors. Experimental Biology and Medicine 229 182-193.
14. Coleman DL 2010 A historical perspective on leptin. Nature Medicine 16 1097-1099. (doi:10.1038/nm1010-1097)
15. Diehn M, Cho RW & Clarke MF 2009 Therapeutic implications of the cancer stem cell hypothesis. Seminars in Radiation Oncology 19 78-86. (doi:10.1016/j.semradonc.2008.11.002)
16. Dogan S, Hu X, Zhang Y, Maihle NJ, Grande JP &Cleary MP 2007 Effects of high-fat diet and/or body weight on mammary tumor leptin and apoptosis signaling pathways in MMTV-TGF-alpha mice. Breast Cancer Research 9 R91. (doi:10.1186/bcr1840)
17. Fiorio E, Mercanti A, Terrasi M, Micciolo R, Remo A, Auriemma A, Molino A, Parolin V, Di Stefano B, Bonetti F et al. 2008 Leptin/HER2 crosstalk in breast cancer: in vitro study and preliminary in vivo analysis. BMC Cancer 8 305. (doi:10.1186/1471-2407-8-305)
18. Flegal KM, Carroll MD, Ogden CL & Johnson CL 2002 Prevalence and trends in obesity among US adults, 1999-2000. Journal of the American Medical Association 288 1723-1727. (doi:10.1001/jama.288.14.1723)
19. Flegal KM, Ogden CL & Carroll MD 2004 Prevalence and trends in overweight in Mexican-American adults and children. Nutrition Reviews 62 S144-S148. (doi:10.1111/j.1753-4887.2004.tb00085.x)
20. Friedman JM 1998 Leptin, leptin receptors, and the control of body weight. Nutrition Reviews 56 s38-s46 (discussion s54-s75). (doi:10.1111/j.1753- 4887.1998.tb01685.x)
21. Garofalo C, Koda M, Cascio S, Sulkowska M, Kanczuga-Koda L, Golaszewska J, Russo A, Sulkowski S &Surmacz E 2006 Increased expression of leptin and the leptin receptor as a marker of breast cancer progression: possible role of obesity-related stimuli. Clinical Cancer Research 12 1447-1453. (doi:10.1158/1078-0432.CCR-05-1913)
22. Gonzalez RR, Cherfils S, Escobar M, Yoo JH, Carino C, Styer AK, Sullivan BT, Sakamoto H, Olawaiye A, Serikawa T et al. 2006 Leptin signaling promotes the growth of mammary tumors and increases the expression of vascular endothelial growth factor (VEGF) and its receptor type two (VEGF-R2). Journal of Biological Chemistry 281 26320-26328. (doi:10.1074/jbc.M601991200)
23. Halberg N, Wernstedt-Asterholm I & Scherer PE 2008 The adipocyte as an endocrine cell. Endocrinology and Metabolism Clinics of North America 37 753-768 x-xi. (doi:10.1016/j.ecl.2008.07.002)
24. Haslam DW & James WP 2005 Obesity. Lancet 366 1197-1209. (doi:10.1016/S0140-6736(05)67483-1)
25. He X, Wang Y, Zhu J, Orloff M & Eng C 2011 Resveratrol enhances the anti-tumor activity of the mTOR inhibitor rapamycin in multiple breast cancer cell lines mainly by suppressing rapamycin-induced AKT signaling. Cancer Letters 301 168-176. (doi:10.1016/j.canlet.2010.11.012)
26. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, Rasmussen KE, Jones LP, Assefnia S, Chandrasekharan S et al. 2007 Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biology 8 R76. (doi:10.1186/gb-2007-8-5-r76)
27. Hu Y & Smyth GK 2009 ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. Journal of Immunological Methods 347 70-78. (doi:10.1016/j.jim.2009.06.008)
28. Hu X, Juneja SC, Maihle NJ & Cleary MP 2002 Leptin - a growth factor in normal and malignant breast cells and for normal mammary gland development. Journal of the National Cancer Institute 94 1704-1711. (doi:10.1093/jnci/94.22. 1704)
29. Huber KE, Carey LA & Wazer DE 2009 Breast cancer molecular subtypes in patients with locally advanced disease: impact on prognosis, patterns of recurrence, and response to therapy. Seminars in Radiation Oncology 19 204-210. (doi:10.1016/j.semradonc.2009.05.004)
30. Hummel KP, Dickie MM & Coleman DL 1966 Diabetes, a new mutation in the mouse. Science 153 1127-1128. (doi:10.1126/science.153.3740.1127)
31. Ingalls AM, Dickie MM & Snell GD 1950 Obese, a new mutation in the house mouse. Journal of Heredity 41 317-318.
32. Ishikawa M, Kitayama J & Nagawa H 2004 Enhanced expression of leptin and leptin receptor (OB-R) in human breast cancer. Clinical Cancer Research 10 4325-4331. (doi:10.1158/1078-0432.CCR-03-0749)
33. Khramtsov AI, Khramtsova GF, Tretiakova M, Huo D, Olopade OI & Goss KH 2010 Wnt/beta-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. American Journal of Pathology 176 2911-2920. (doi:10.2353/ajpath.2010.091125)
34. Li Y, Hively WP & Varmus HE 2000 Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 19 1002-1009. (doi:10.1038/sj.onc.1203273)
35. Liu S & Wicha MS 2010 Targeting breast cancer stem cells. Journal of Clinical Oncology 28 4006-4012. (doi:10.1200/JCO.2009.27.5388)
36. Loi S, Milne RL, Friedlander ML, McCredie MR, Giles GG, Hopper JL & Phillips KA 2005 Obesity and outcomes in premenopausal and postmenopausal breast cancer. Cancer Epidemiology, Biomarkers &Prevention 14 1686-1691. (doi:10.1158/1055-9965.EPI-05-0042)
37. Maccio A, Madeddu C, Gramignano G, Mulas C, Floris C, Massa D, Astara G, Chessa P & Mantovani G 2010 Correlation of body mass index and leptin with tumor size and stage of disease in hormone-dependent postmenopausal breast cancer: preliminary results and therapeutic implications. Journal of Molecular Medicine 88 677-686. (doi:10.1007/s00109-010-0611-8)
38. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M et al. 2008 The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133 704-715. (doi:10.1016/j.cell.2008.03.027)
39. Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT et al. 2008 Epidemiology of basal-like breast cancer. Breast Cancer Research and Treatment 109 123-139. (doi:10.1007/s10549-007-9632-6)
40. Miyoshi Y, Funahashi T, Tanaka S, Taguchi T, Tamaki Y, Shimomura I & Noguchi S 2006 High expression of leptin receptor mRNA in breast cancer tissue predicts poor prognosis for patients with high, but not low, serum leptin levels. International Journal of Cancer 118 1414-1419. (doi:10.1002/ijc.21543)
41. Myers MG, Cowley MA & Munzberg H 2008 Mechanisms of leptin action and leptin resistance. Annual Review of Physiology 70 537-556. (doi:10.1146/ annurev.physiol.70.113006.100707)
42. Nunez NP, Perkins SN, Smith NC, Berrigan D, Berendes DM, Varticovski L, Barrett JC & Hursting SD 2008 Obesity accelerates mouse mammary tumor growth in the absence of ovarian hormones. Nutrition and Cancer 60 534-541. (doi:10.1080/01635580801966195)
43. Nusse R, Fuerer C, Ching W, Harnish K, Logan C, Zeng A, ten Berge D & Kalani Y 2008 Wnt signaling and stem cell control. Cold Spring Harbor Symposia on Quantitative Biology 73 59-66. (doi:10.1101/sqb.2008.73.035)
44. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ & Flegal KM 2006 Prevalence of overweight and obesity in the United States, 1999-2004. Journal of the American Medical Association 295 1549-1555. (doi:10.1001/jama. 295.13.1549)
45. Park J, Kusminski CM, Chua SC & Scherer PE 2010 Leptin receptor signaling supports cancer cell metabolism through suppression of mitochondrial respiration in vivo. American Journal of Pathology 177 3133-3144. (doi:10.2353/ajpath.2010.100595)
46. Rene Gonzalez R, Watters A, Xu Y, Singh UP, Mann DR, Rueda BR & Penichet ML 2009 Leptin-signaling inhibition results in efficient anti-tumor activity in estrogen receptor positive or negative breast cancer. Breast Cancer Research 11 R36. (doi:10.1186/bcr2321)
47. Rich JN & Eyler CE 2008 Cancer stem cells in brain tumor biology. Cold Spring Harbor Symposia on Quantitative Biology 73 411-420. (doi:10.1101/sqb.2008.73.060)
48. Rosen JM & Jordan CT 2009 The increasing complexity of the cancer stem cell paradigm. Science 324 1670-1673. (doi:10.1126/science.1171837)
49. Saxena NK, Taliaferro-Smith L, Knight BB, Merlin D, Anania FA, O'Regan RM & Sharma D 2008 Bidirectional crosstalk between leptin and insulin-like growth factor-I signaling promotes invasion and migration of breast cancer cells via transactivation of epidermal growth factor receptor. Cancer Research 68 9712-9722. (doi:10.1158/0008-5472.CAN-08-1952)
50. Spiegelman BM & Flier JS 2001 Obesity and the regulation of energy balance. Cell 104 531-543. (doi:10.1016/S0092-8674(01)00240-9)
51. Surmacz E 2007 Obesity hormone leptin: a new target in breast cancer? Breast Cancer Research 9 301. (doi:10.1186/bcr1638)
52. Thompson CI, Kreider JW, Black PL, Schmidt TJ &Margules DL 1983 Genetically obese mice: resistance to metastasis of B16 melanoma and enhanced T-lymphocyte mitogenic responses. Science 220 1183-1185. (doi:10.1126/science. 6602379)
53. Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ & Visvader JE 2008 The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Research 68 7711-7717. (doi:10.1158/0008-5472.CAN-08-1949)
54. Visvader JE & Smith GH 2010 Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harbor Perspectives in Biology 3 a004879. (doi:10.1101/cshperspect.a004879)
55. Zhang M, Atkinson RL & Rosen JM 2010 Selective targeting of radiation-resistant tumor-initiating cells. PNAS 107 3522-3527. (doi:10.1073/pnas.0910179107)