Bone marrow adipocytes promote tumor growth in bone via FABP4-dependent mechanisms

Oncotarget

Volumn 4, Issue 11, 2013, Pages 2108-2123

  Herroon, Mackenzie K ^a   Rajagurubandara, Erandi ^a   Hardaway, Aimalie L ^a   Powell, Katelyn ^a   Turchick, Audrey ^b   Feldmann, Daniel ^a   Podgorski, Izabela ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone marrow adipocytes; Bone metastasis; Breast cancer; Heme oxygenase 1; Interleukin 1 ; Prostate cancer

Indexed keywords

CD36 ANTIGEN; FATTY ACID BINDING PROTEIN 4; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; BONE METASTASIS; CANCER PATIENT; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; UPREGULATION;

ADIPOCYTES; ANIMALS; BONE MARROW; BONE NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; FATTY ACID-BINDING PROTEINS; HUMANS; INTERLEUKIN-1BETA; MALE; MICE; PPAR GAMMA; PROSTATIC NEOPLASMS; TRANSFECTION; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84890221321     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1482     Document Type: Article

References (73)

1. Bassett WW, Cooperberg MR, Sadetsky N, Silva S, DuChane J, Pasta DJ, Chan JM, Anast JW, Carroll PR and Kane CJ. Impact of obesity on prostate cancer recurrence after radical prostatectomy: data from CaPSURE. Urology. 2005; 66(5):1060-1065.
2. Freedland SJ, Banez LL, Sun LL, Fitzsimons NJ and Moul JW. Obese men have higher-grade and larger tumors: an analysis of the duke prostate center database. Prostate cancer and prostatic diseases. 2009; 12(3):259-263.
3. Gong Z, Neuhouser ML, Goodman PJ, Albanes D, Chi C, Hsing AW, Lippman SM, Platz EA, Pollak MN, Thompson IM and Kristal AR. Obesity, diabetes, and risk of prostate cancer: results from the prostate cancer prevention trial. Cancer Epidemiol Biomarkers Prev. 2006; 15(10):1977-1983.
4. Scosyrev E, Messing EM, Mohile S, Golijanin D and Wu G. Prostate cancer in the elderly: frequency of advanced disease at presentation and disease-specific mortality. Cancer. 2012; 118(12):3062-3070.
5. Keto CJ, Aronson WJ, Terris MK, Presti JC, Kane CJ, Amling CL and Freedland SJ. Obesity is associated with castration-resistant disease and metastasis in men treated with androgen deprivation therapy after radical prostatectomy: results from the SEARCH database. BJU Int. 2012; 110(4):492-498.
6. Duque G. Bone and fat connection in aging bone. Current opinion in rheumatology. 2008; 20(4):429-434.
7. Lecka-Czernik B, Rosen CJ and Kawai M. Skeletal aging and the adipocyte program: New insights from an "old" molecule. Cell Cycle. 2010; 9(18):3648-3654.
8. Rosen CJ, Ackert-Bicknell C, Rodriguez JP and Pino AM. Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr. 2009; 19(2):109-124.
9. Strotmeyer ES and Cauley JA. Diabetes mellitus, bone mineral density, and fracture risk. Curr Opin Endocrinol Diabetes Obes. 2007; 14(6):429-435.
10. Schwartz AV and Sellmeyer DE. Diabetes, fracture, and bone fragility. Curr Osteoporos Rep. 2007; 5(3):105-111.
11. Paula FJ and Rosen CJ. Obesity, diabetes mellitus and last but not least, osteoporosis. Arq Bras Endocrinol Metabol. 2010; 54(2):150-157.
12. Rosen CJ and Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nature clinical practice. 2006; 2(1):35-43.
13. Cao JJ, Sun L and Gao H. Diet-induced obesity alters bone remodeling leading to decreased femoral trabecular bone mass in mice. Ann N Y Acad Sci. 2010; 1192:292-297.
14. Halade GV, El Jamali A, Williams PJ, Fajardo RJ and Fernandes G. Obesity-mediated inflammatory microenvironment stimulates osteoclastogenesis and bone loss in mice. Exp Gerontol. 2011; 46(1):43-52.
15. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T and Kassem M. Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology. 2001; 2(3):165-171.
16. Meunier P, Aaron J, Edouard C and Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res. 1971; 80:147-154.
17. Vande Berg BC, Malghem J, Lecouvet FE and Maldague B. Magnetic resonance imaging of normal bone marrow. Eur Radiol. 1998; 8(8):1327-1334.
18. Wang D. Magnetic resonance imaging of bone marrow: a review - Part I. Journal of American Osteopathic College of Radiology. 2012; 1(2):2-12.
19. Brown MD, Hart CA, Gazi E, Bagley S and Clarke NW. Promotion of prostatic metastatic migration towards human bone marrow stoma by Omega 6 and its inhibition by Omega 3 PUFAs. British journal of cancer. 2006; 94(6):842-853.
20. Gazi E, Gardner P, Lockyer NP, Hart CA, Brown MD and Clarke NW. Direct evidence of lipid translocation between adipocytes and prostate cancer cells with imaging FTIR microspectroscopy. Journal of lipid research. 2007; 48(8):1846-1856.
21. Lecka-Czernik B. Marrow fat metabolism is linked to the systemic energy metabolism. Bone. 2011.
22. Halade GV, Rahman MM, Williams PJ and Fernandes G. High fat diet-induced animal model of age-associated obesity and osteoporosis. J Nutr Biochem. 2010; 21(12):1162-1169.
23. Trottier MD, Naaz A, Li Y and Fraker PJ. Enhancement of hematopoiesis and lymphopoiesis in diet-induced obese mice. Proc Natl Acad Sci U S A. 2012; 109(20):7622-7629.
24. Tokuda Y, Satoh Y, Fujiyama C, Toda S, Sugihara H and Masaki Z. Prostate cancer cell growth is modulated by adipocyte-cancer cell interaction. BJU Int. 2003; 91(7):716-720.
25. Nieman K, Kenny H, Penicka C, Ladanyi A, Buell-Gutbrod R, Zillhardt M, Romero I, Carey M, Mills G, Hotamisligil G, Yamada S, Peter M, Gwin K and Lengyel E. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nature medicine. 2011; 17(11):1498-1503.
26. Nieman K, Romero I, Van Houten B and Lengyel E. Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochim Biophys Acta. 2013; Epub ahead of print.
27. Furuhashi M and Hotamisligil GS. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov. 2008; 7(6):489-503.
28. Makowski L and Hotamisligil GS. Fatty acid binding proteins--the evolutionary crossroads of inflammatory and metabolic responses. J Nutr. 2004; 134(9):2464S-2468S.
29. Lowe CE, O'Rahilly S and Rochford JJ. Adipogenesis at a glance. Journal of cell science. 2011; 124(Pt 16):2681-2686.
30. Ayers SD, Nedrow KL, Gillilan RE and Noy N. Continuous nucleocytoplasmic shuttling underlies transcriptional activation of PPARgamma by FABP4. Biochemistry. 2007; 46(23):6744-6752.
31. Strand DW, Jiang M, Murphy TA, Yi Y, Konvinse KC, Franco OE, Wang Y, Young JD and Hayward SW. PPARgamma isoforms differentially regulate metabolic networks to mediate mouse prostatic epithelial differentiation. Cell Death Dis. 2012; 3:e361.
32. Jiang M, Jerome WG and Hayward SW. Autophagy in nuclear receptor PPARgamma-deficient mouse prostatic carcinogenesis. Autophagy. 2010; 6(1):175-176.
33. Daynes RA and Jones DC. Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol. 2002; 2(10):748-759.
34. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK and Sethi G. Inflammation and cancer: how hot is the link? Biochem Pharmacol. 2006; 72(11):1605-1621.
35. Apte RN, Krelin Y, Song X, Dotan S, Recih E, Elkabets M, Carmi Y, Dvorkin T, White RM, Gayvoronsky L, Segal S and Voronov E. Effects of micro-environment- and malignant cell-derived interleukin-1 in carcinogenesis, tumour invasiveness and tumour-host interactions. Eur J Cancer. 2006; 42(6):751-759.
36. Elaraj DM, Weinreich DM, Varghese S, Puhlmann M, Hewitt SM, Carroll NM, Feldman ED, Turner EM and Alexander HR. The role of interleukin 1 in growth and metastasis of human cancer xenografts. Clin Cancer Res. 2006; 12(4):1088-1096.
37. Weinreich DM, Elaraj DM, Puhlmann M, Hewitt SM, Carroll NM, Feldman ED, Turner EM, Spiess PJ and Alexander HR. Effect of interleukin 1 receptor antagonist gene transduction on human melanoma xenografts in nude mice. Cancer Res. 2003; 63(18):5957-5961.
38. Was H, Dulak J and Jozkowicz A. Heme oxygenase-1 in tumor biology and therapy. Curr Drug Targets. 2010; 11(12):1551-1570.
39. Nuhn P, Kunzli BM, Hennig R, Mitkus T, Ramanauskas T, Nobiling R, Meuer SC, Friess H and Berberat PO. Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo. Mol Cancer. 2009; 8:37.
40. Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Kunzli B, Autschbach F, Meuer S, Buchler MW and Friess H. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res. 2005; 11(10):3790-3798.
41. Kweon MH, Adhami VM, Lee JS and Mukhtar H. Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem. 2006; 281(44):33761-33772.
42. Herroon MK, Rajagurubandara E, Rudy DL, Chalasani A, Hardaway AL and Podgorski I. Macrophage cathepsin K promotes prostate tumor progression in bone. Oncogene. 2012.
43. Hancke K, Grubeck D, Hauser N, Kreienberg R and Weiss JM. Adipocyte fatty acid-binding protein as a novel prognostic factor in obese breast cancer patients. Breast Cancer Res Treat. 2010; 119(2):367-367.
44. Manabe Y, Toda S, Miyazaki K and Sugihara H. Mature adipocytes, but not preadipocytes, promote the growth of breast carcinoma cells in collagen gel matrix culture through cancer-stromal cell interactions. J Pathol. 2003; 201(2):221-228.
45. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt MR, Romero IL, Carey MS, Mills GB, Hotamisligil GS, Yamada SD, Peter ME, Gwin K and Lengyel E. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nature medicine. 2011; 17(11):1498-1503.
46. Brown MD, Hart C, Gazi E, Gardner P, Lockyer N and Clarke N. Influence of omega-6 PUFA arachidonic acid and bone marrow adipocytes on metastatic spread from prostate cancer. British journal of cancer. 2010; 102(2):403-413.
47. Huang M, Narita S, Numakura K, Tsuruta H, Saito M, Inoue T, Horikawa Y, Tsuchiya N and Habuchi T. A high-fat diet enhances proliferation of prostate cancer cells and activates MCP-1/CCR2 signaling. Prostate. 2012; 72(16):1779-1788.
48. Llaverias G, Danilo C, Wang Y, Witkiewicz A, Daumer K, Lisanti M and Frank P. A Western-type diet accelerates tumor progression in an autochthonous mouse model of prostate cancer. Am J Pathol. 2010; 177(6):3180-3191.
49. Park H, Kim M, Kwon GT, Lim do Y, Yu R, Sung MK, Lee KW, Daily JW, 3rd and Park JH. A high-fat diet increases angiogenesis, solid tumor growth, and lung metastasis of CT26 colon cancer cells in obesity-resistant BALB/c mice. Mol Carcinog. 2012; 51(11):869-880.
50. Lawrence JW, Kroll DJ and Eacho PI. Ligand-dependent interaction of hepatic fatty acid-binding protein with the nucleus. Journal of lipid research. 2000; 41(9):1390-1401.
51. Gillilan RE, Ayers SD and Noy N. Structural basis for activation of fatty acid-binding protein 4. J Mol Biol. 2007; 372(5):1246-1260.
52. Sacca P, Meiss R, Casas G, Mazza O, Calvo JC, Navone N and Vazquez E. Nuclear translocation of haeme oxygenase-1 is associated to prostate cancer. British journal of cancer. 2007; 97(12):1683-1689.
53. Furuhashi M, Tuncman G, Gorgun CZ, Makowski L, Atsumi G, Vaillancourt E, Kono K, Babaev VR, Fazio S, Linton MF, Sulsky R, Robl JA, Parker RA and Hotamisligil GS. Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature. 2007; 447(7147):959-965.
54. Perera RJ, Marcusson EG, Koo S, Kang X, Kim Y, White N and Dean NM. Identification of novel PPARgamma target genes in primary human adipocytes. Gene. 2006; 369:90-99.
55. Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, Wang YY, Meulle A, Salles B, Le Gonidec S, Garrido I, Escourrou G, Valet P and Muller C. Cancer-associated adipocytes xhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011; 71(7):2455-2465.
56. Nieman KM, Romero IL, Van Houten B and Lengyel E. Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochim Biophys Acta. 2013.
57. Gimble JM and Nuttall ME. Bone and fat: old questions, new insights. Endocrine. 2004; 23(2-3):183-188.
58. Nuttall ME and Gimble JM. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Current opinion in pharmacology. 2004; 4(3):290-294.
59. Liu Y. Fatty acid oxidation is a dominant bioenergetic pathway in prostate cancer. Prostate cancer and prostatic diseases. 2006; 9(3):230-234.
60. Martinez-Outschoorn UE, Sotgia F and Lisanti MP. Power surge: supporting cells "fuel" cancer cell mitochondria. Cell metabolism. 2012; 15(1):4-5.
61. Nakajima EC and Van Houten B. Metabolic symbiosis in cancer: Refocusing the Warburg lens. Mol Carcinog. 2013; 52(5):329-337.
62. Hauser S, Adelmant G, Sarraf P, Wright HM, Mueller E and Spiegelman BM. Degradation of the peroxisome proliferator-activated receptor gamma is linked to ligand-dependent activation. J Biol Chem. 2000; 275(24):18527-18533.
63. Jiang M, Strand DW, Franco OE, Clark PE and Hayward SW. PPARgamma: a molecular link between systemic metabolic disease and benign prostate hyperplasia. Differentiation. 2011; 82(4-5):220-236.
64. Elmasri H, Karaaslan C, Teper Y, GhelfiE, Weng M, Ince T, Kozakewich H, BischoffJ and Cataltepe S. Elmasri H, Karaaslan C, Teper Y, GhelfiE, Weng M, Ince TA, Kozakewich H, BischoffJ, Cataltepe S. FASEB Journal. 2009; 23(11):3865-3873.
65. Cataltepe O, Arikan MC, GhelfiE, Karaaslan C, Ozsurekci Y, Dresser K, Li Y, Smith TW and Cataltepe S. Fatty acid binding protein 4 is expressed in distinct endothelial and non-endothelial cell populations in glioblastoma. Neuropathol Appl Neurobiol. 2012; 38(5):400-410.
66. Shankar E, Vykhovanets EV, Vykhovanets OV, Maclennan GT, Singh R, Bhaskaran N, Shukla S and Gupta S. High-fat diet activates pro-inflammatory response in the prostate through association of Stat-3 and NF-kappaB. Prostate. 2012; 72(3):233-243.
67. Suburu J and Chen YQ. Lipids and prostate cancer. Prostaglandins Other Lipid Mediat. 2012; 98(1-2):1-10.
68. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF and Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Investigative urology.1979; 17(1):16-23.
69. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, Chu G, Liu ZR, Zhou BP, Huang WC and Chung LW. Epithelial to mesenchymal transition (EMT) in human prostate cancer: lessons learned from ARCaP model. Clinical&experimental metastasis. 2008; 25(6):601-610.
70. Yoneda T, Williams PJ, Hiraga T, Niewolna M and Nishimura R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast ancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res. 2001; 16(8):1486-1495.
71. Podgorski I, Linebaugh BE, Koblinski JE, Rudy DL, Herroon MK, Olive MB and Sloane BF. Bone marrow-derived cathepsin K cleaves SPARC in bone metastasis. Am J Pathol. 2009; 175(3):1255-1269.
72. Downs TR and Wilfinger WW. Fluorometric quantification of DNA in cells and tissue. Analytical biochemistry. 1983; 131(2):538-547.
73. Podgorski I, Linebaugh BE, Sameni M, Jedeszko C, Bhagat S, Cher ML and Sloane BF. Bone microenvironment modulates expression and activity of cathepsin B in prostate cancer. Neoplasia. 2005; 7(3):207-223.