Adipose tissue attracts and protects acute lymphoblastic leukemia cells from chemotherapy

Leukemia Research

Volumn 37, Issue 5, 2013, Pages 503-509

  Pramanik, Rocky ^a,b   Sheng, Xia ^a   Ichihara, Brian ^a   Heisterkamp, Nora ^a,b   Mittelman, Steven D ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Acute lymphoblastic leukemia; Adipocytes; ALL; AMD3100; C X C chemokine receptor type 4; CXCR4; Microenvironment; SDF 1 , stromal derived factor 1 alpha

Indexed keywords

DAUNORUBICIN; STROMAL CELL DERIVED FACTOR 1ALPHA; VINCRISTINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER RECURRENCE; CANCER RESISTANCE; CANCER RISK; CELL MIGRATION; CELL PROTECTION; CELL SURVIVAL; CHEMOTAXIS; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RISK ASSESSMENT; TUMOR MICROENVIRONMENT;

3T3-L1 CELLS; ADIPOSE TISSUE; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; DAUNORUBICIN; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; NEOPLASM TRANSPLANTATION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; TRANSPLANTATION, ISOGENEIC; TUMOR MICROENVIRONMENT; VINCRISTINE;

EID: 84875908777     PISSN: 01452126     EISSN: 18735835     Source Type: Journal    
DOI: 10.1016/j.leukres.2012.12.013     Document Type: Article

References (50)

1. Pui C.H., Carroll W.L., Meshinchi S., Arceci R.J. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol 2011, 29:551-565.
2. Fielding A. The treatment of adults with acute lymphoblastic leukemia. Hematology Am Soc Hematol Educ Program 2008, 381-389.
3. Buchanan G.R. Diagnosis and management of relapse in acute lymphoblastic leukemia. Hematol Oncol Clin North Am 1990, 4:971-995.
4. Kurtova A.V., Balakrishnan K., Chen R., Ding W., Schnabl S., Quiroga M.P., et al. Diverse marrow stromal cells protect CLL cells from spontaneous and drug-induced apoptosis: development of a reliable and reproducible system to assess stromal cell adhesion-mediated drug resistance. Blood 2009, 114:4441-4450.
5. Mudry R.E., Fortney J.E., York T., Hall B.M., Gibson L.F. Stromal cells regulate survival of B-lineage leukemic cells during chemotherapy. Blood 2000, 96:1926-1932.
6. Iyengar P., Combs T.P., Shah S.J., Gouon-Evans V., Pollard J.W., Albanese C., et al. Adipocyte-secreted factors synergistically promote mammary tumorigenesis through induction of anti-apoptotic transcriptional programs and proto-oncogene stabilization. Oncogene 2003, 22:6408-6423.
7. Bartucci M., Svensson S., Ricci-Vitiani L., Dattilo R., Biffoni M., Signore M., et al. Obesity hormone leptin induces growth and interferes with the cytotoxic effects of 5-fluorouracil in colorectal tumor stem cells. Endocr Relat Cancer 2010, 17:823-833.
8. Behan J.W., Yun J.P., Proektor M.P., Ehsanipour E.A., Arutyunyan A., Moses A.S., et al. Adipocytes impair leukemia treatment in mice. Cancer Res 2009, 69:7867-7874.
9. van Kruijsdijk R.C., van der W.E., Visseren F.L. Obesity and cancer: the role of dysfunctional adipose tissue. Cancer Epidemiol Biomarkers Prev 2009, 18:2569-2578.
10. Wolin K.Y., Carson K., Colditz G.A. Obesity and cancer. Oncologist 2010, 15:556-565.
11. Roberts D.L., Dive C., Renehan A.G. Biological mechanisms linking obesity and cancer risk: new perspectives. Annu Rev Med 2010, 61:301-316.
12. Renehan A.G., Roberts D.L., Dive C. Obesity and cancer: pathophysiological and biological mechanisms. Arch Physiol Biochem 2008, 114:71-83.
13. Calle E.E., Rodriguez C., Walker-Thurmond K., Thun M.J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003, 348:1625-1638.
14. Butturini A., Vignetti M., Gubbiotti S., Meloni G., Recchia M., Di Raimondo F., et al. Obesity independently predicts event free survival (EFS) in adults with BCR-ABL-negative acute lymphoblastic leukemia (ALL), a retrospective analysis of two GIMEMA studies. ASH Ann. Meet. Abstr. 2005, 106:1828.
15. Butturini A.M., Dorey F.J., Lange B.J., Henry D.W., Gaynon P.S., Fu C., et al. Obesity and outcome in pediatric acute lymphoblastic leukemia. J Clin Oncol 2007, 25:2063-2069.
16. Mishra S., Zhang B., Groffen J., Heisterkamp N. A farnesyltransferase inhibitor increases survival of mice with very advanced stage acute lymphoblastic leukemia/lymphoma caused by P190 Bcr/Abl. Leukemia 2004, 18:23-28.
17. Fei F., Stoddart S., Muschen M., Kim Y.M., Groffen J., Heisterkamp N. Development of resistance to dasatinib in Bcr/Abl-positive acute lymphoblastic leukemia. Leukemia 2010, 24:813-820.
18. Parameswaran R., Muschen M., Kim Y.M., Groffen J., Heisterkamp N. A functional receptor for B-cell-activating factor is expressed on human acute lymphoblastic leukemias. Cancer Res 2010, 70:4346-4356.
19. Darimont C., Zbinden I., Avanti O., Leone-Vautravers P., Giusti V., Burckhardt P., et al. Reconstitution of telomerase activity combined with HPV-E7 expression allow human preadipocytes to preserve their differentiation capacity after immortalization. Cell Death Differ 2003, 10:1025-1031.
20. Manabe A., Murti K.G., Coustan-Smith E., Kumagai M., Behm F.G., Raimondi S.C., et al. Adhesion-dependent survival of normal and leukemic human B lymphoblasts on bone marrow stromal cells. Blood 1994, 83:758-766.
21. Nishigaki H., Ito C., Manabe A., Kumagai M., Coustan-Smith E., Yanishevski Y., et al. Prevalence and growth characteristics of malignant stem cells in B-lineage acute lymphoblastic leukemia. Blood 1997, 89:3735-3744.
22. Kintscher U., Hartge M., Hess K., Foryst-Ludwig A., Clemenz M., Wabitsch M., et al. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 2008, 28:1304-1310.
23. Robker R.L., Collins R.G., Beaudet A.L., Mersmann H.J., Smith C.W. Leukocyte migration in adipose tissue of mice null for ICAM-1 and Mac-1 adhesion receptors. Obes Res 2004, 12:936-940.
24. Bowman W.P., Larsen E.L., Devidas M., Linda S.B., Blach L., Carroll A.J., et al. Augmented therapy improves outcome for pediatric high risk acute lymphocytic leukemia: results of Children's Oncology Group trial P9906. Pediatr Blood Cancer 2011.
25. Baggiolini M., Chemokines Leukocyte traffic. Nature 1998, 392:565-568.
26. Moser B., Loetscher P. Lymphocyte traffic control by chemokines. Nat Immunol 2001, 2:123-128.
27. Juarez J., Bradstock K.F., Gottlieb D.J., Bendall L.J. Effects of inhibitors of the chemokine receptor CXCR4 on acute lymphoblastic leukemia cells in vitro. Leukemia 2003, 17:1294-1300.
28. Bleul C.C., Fuhlbrigge R.C., Casasnovas J.M., Aiuti A., Springer T.A. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 1996, 184:1101-1109.
29. Mohle R., Bautz F., Rafii S., Moore M.A., Brugger W., Kanz L. The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 1998, 91:4523-4530.
30. Peled A., Kollet O., Ponomaryov T., Petit I., Franitza S., Grabovsky V., et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 2000, 95:3289-3296.
31. Hosokawa Y., Hosokawa I., Ozaki K., Nakae H., Murakami K., Miyake Y., et al. CXCL12 and CXCR4 expression by human gingival fibroblasts in periodontal disease. Clin Exp Immunol 2005, 141:467-474.
32. Lai P., Li T., Yang J., Xie C., Zhu X., Xie H., et al. Upregulation of stromal cell-derived factor 1 (SDF-1) expression in microvasculature endothelial cells in retinal ischemia-reperfusion injury. Graefes Arch Clin Exp Ophthalmol 2008, 246:1707-1713.
33. Choi S., Kim J., Yea K., Suh P.G., Kim J., Ryu S.H. Targeted label-free quantitative analysis of secretory proteins from adipocytes in response to oxidative stress. Anal Biochem 2010, 401:196-202.
34. Caspar-Bauguil S., Cousin B., Galinier A., Segafredo C., Nibbelink M., Andre M., et al. Adipose tissues as an ancestral immune organ: site-specific change in obesity. FEBS Lett 2005, 579:3487-3492.
35. Winer D.A., Winer S., Shen L., Wadia P.P., Yantha J., Paltser G., et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011, 17:610-617.
36. Caspar-Bauguil S., Cousin B., Andre M., Nibbelink M., Galinier A., Periquet B., et al. Weight-dependent changes of immune system in adipose tissue: importance of leptin. Exp Cell Res 2006, 312:2195-2202.
37. Duffaut C., Galitzky J., Lafontan M., Bouloumie A. Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochem Biophys Res Commun 2009, 384:482-485.
38. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003, 112:1821-1830.
39. Fenton J.I., Nunez N.P., Yakar S., Perkins S.N., Hord N.G., Hursting S.D. Diet-induced adiposity alters the serum profile of inflammation in C57BL/6N mice as measured by antibody array. Diabetes Obes Metab 2009, 11:343-354.
40. Jung C., Fischer N., Fritzenwanger M., Pernow J., Brehm B.R., Figulla H.R. Association of waist circumference, traditional cardiovascular risk factors, and stromal-derived factor-1 in adolescents. Pediatr Diabetes 2009, 10:329-335.
41. Spiegel A., Kollet O., Peled A., Abel L., Nagler A., Bielorai B., et al. Unique SDF-1-induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood 2004, 103:2900-2907.
42. Maitra A., McKenna R.W., Weinberg A.G., Schneider N.R., Kroft S.H. Precursor B-cell lymphoblastic lymphoma. A study of nine cases lacking blood and bone marrow involvement and review of the literature. Am J Clin Pathol 2001, 115:868-875.
43. Lozzi G.P., Massone C., Citarella L., Kerl H., Cerroni L. Rimming of adipocytes by neoplastic lymphocytes: a histopathologic feature not restricted to subcutaneous T-cell lymphoma. Am J Dermatopathol 2006, 28:9-12.
44. Behan J.W., Avramis V.I., Yun J.P., Louie S.G., Mittelman SD Diet-induced obesity alters vincristine pharmacokinetics in blood and tissues of mice. Pharmacol Res 2010.
45. Ottaiano A., di P.A., Napolitano M., Pisano C., Pignata S., Tatangelo F., et al. Inhibitory effects of anti-CXCR4 antibodies on human colon cancer cells. Cancer Immunol Immunother 2005, 54:781-791.
46. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
47. Taichman R.S., Cooper C., Keller E.T., Pienta K.J., Taichman N.S., McCauley L.K. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002, 62:1832-1837.
48. Burger J.A., Peled A. CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 2009, 23:43-52.
49. Tavor S., Petit I. Can inhibition of the SDF-1/CXCR4 axis eradicate acute leukemia?. Semin Cancer Biol 2010.
50. Parameswaran R., Yu M., Lim M., Groffen J., Heisterkamp N. Combination of drug therapy in acute lymphoblastic leukemia with a CXCR4 antagonist. Leukemia 2011.