Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 9, 2015

Adiponectin as a biomarker linking obesity and adiposopathy to hematologic malignancies

  • Maria Dalamaga EMAIL logo and Gerasimos S. Christodoulatos

Abstract

Higher body mass index and adiposopathy have been associated with increased risk of hematologic malignancies such as leukemia, multiple myeloma, myeloproliferative disorders, Hodgkin’s and non-Hodgkin’s lymphoma, and myelodysplastic syndromes. Adiponectin is a multimeric protein of the white adipose tissue presenting anti-inflammatory, insulin-sensitizing, anti-atherogenic, cardioprotective, and anti-neoplastic properties. Its anti-neoplastic actions are manifested via two mechanisms: (i) direct action on tumor cells by enhancing receptor-mediated signaling pathways and (ii) indirect action by regulating inflammatory responses, influencing cancer angiogenesis, and modulating insulin sensitivity at the target tissue site. In the bone marrow milieu, adiponectin and its main receptors are expressed by the majority of bone marrow stromal cell populations influencing hematopoietic stem cells function. Adiponectin may represent a molecular mediator relating adiposopathy with leukemogenesis and myelomagenesis. Several epidemiological studies conducted to date relate hypoadiponectinemia to the risk of myeloid-derived hematopoietic cancer and multiple myeloma. Adiponectin may be a promising biomarker with potential diagnostic and prognostic utility in determining the likelihood of myeloma and leukemia progression in certain cohorts of monoclonal gammopathy of undetermined significance patients and in myeloid hematologic malignancies, respectively. This review summarizes experimental and epidemiologic data regarding the role of adiponectin in hematologic malignancies in the context of adiposopathy. Enhancement of endogenous adiponectin, adiponectin replacement, or manipulation of adiponectin receptor sensitivity may be an attractive goal for prevention and an effective therapeutic strategy against hematopoietic cancer, specifically in overweight/obese individuals. Further studies are required to elucidate the role of the bone marrow microenvironment adiponectin in complex interactions involved in preleukemic and leukemic states.


Corresponding author: Maria Dalamaga, MD, PhD, MS, MPH, Associate Professor, Department of Clinical Biochemistry, Medical School, University of Athens, Karyotaki #29, 15344 Athens, Pallini, Greece, Phone: +30-210-7462624, Fax: +30-210-6082467, E-mail:

References

1. Hubert HB, Feinleib M, McNamara PM, Castelli WP. Obesity as an independent risk factor for cardiovascular disease: a 26-year follow-up of participants in the Framingham Heart Study. Circulation 1983;67:968–77.10.1161/01.CIR.67.5.968Search in Google Scholar

2. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. J Am Med Assoc 2003;289:76–9.10.1001/jama.289.1.76Search in Google Scholar

3. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM. The epidemiology of obesity. Gastroenterology 2007;132:2087–102.10.1053/j.gastro.2007.03.052Search in Google Scholar

4. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008;371:569–78.10.1016/S0140-6736(08)60269-XSearch in Google Scholar

5. Papadavid E, Vlami K, Dalamaga M, Giatrakou S, Theodoropoulos K, Gyftopoulos S, Stavrianeas N, Papiris S, Rigopoulos D. Sleep apnea as a comorbidity in obese psoriasis patients: a cross-sectional study. Do psoriasis characteristics and metabolic parameters play a role? J Eur Acad Dermatol Venereol 2013;27:820–6.10.1111/j.1468-3083.2012.04580.xSearch in Google Scholar

6. Dalamaga M, Diakopoulos KN, Mantzoros CS. The role of adiponectin in cancer: a review of current evidence. Endocr Rev 2012;33:547–94.10.1210/er.2011-1015Search in Google Scholar PubMed PubMed Central

7. Dalamaga M. Interplay of adipokines and myokines in cancer pathophysiology: emerging therapeutic implications. World J Exp Med 2013;3:26–33.10.5493/wjem.v3.i3.26Search in Google Scholar PubMed PubMed Central

8. Larsson SC, Orsini N, Wolk A. Body mass index and pancreatic cancer risk: a meta-analysis of prospective studies. Int J Cancer 2007;120:1993–8.10.1002/ijc.22535Search in Google Scholar PubMed

9. Wiseman M. The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc 2008;67:253–6.10.1017/S002966510800712XSearch in Google Scholar PubMed

10. Hsing AW, Sakoda LC, Chua S, Jr. Obesity, metabolic syndrome, and prostate cancer. Am J Clin Nutr 2007;86:s843–57.10.1093/ajcn/86.3.843SSearch in Google Scholar PubMed

11. Dalamaga M, Migdalis I, Fargnoli JL, Papadavid E, Bloom E, Mitsiades N, Karmaniolas K, Pelecanos N, Tseleni-Balafouta S, Dionyssiou-Asteriou A, Mantzoros CS. Pancreatic cancer expresses adiponectin receptors and is associated with hypoleptinemia and hyperadiponectinemia: a case-control study. Cancer Causes Control 2009;20:625–33.10.1007/s10552-008-9273-zSearch in Google Scholar PubMed PubMed Central

12. Dalamaga M. Obesity, insulin resistance, adipocytokines and breast cancer: new biomarkers and attractive therapeutic targets. World J Exp Med 2013;3:34–42.10.5493/wjem.v3.i3.34Search in Google Scholar PubMed PubMed Central

13. Dalamaga M, Sotiropoulos G, Karmaniolas K, Pelekanos N, Papadavid E, Lekka A. Serum resistin: a biomarker of breast cancer in postmenopausal women? Association with clinicopathological characteristics, tumor markers, inflammatory and metabolic parameters. Clin Biochem 2013;46:584–90.10.1016/j.clinbiochem.2013.01.001Search in Google Scholar PubMed

14. Dalamaga M. Nicotinamide phosphoribosyl-transferase/visfatin: a missing link between overweight/obesity and postmenopausal breast cancer? Potential preventive and therapeutic perspectives and challenges. Med Hypotheses 2012;79:617–21.10.1016/j.mehy.2012.07.036Search in Google Scholar PubMed

15. Dalamaga M, Papadavid E, Vlami K. Unmasking the Janus face of the association between psoriasis, metabolic syndrome and obstructive sleep apnea. Sleep Breath 2013;17:449–50.10.1007/s11325-012-0749-4Search in Google Scholar PubMed

16. van Kruijsdijk RC, van der Wall E, Visseren FL. Obesity and cancer: the role of dysfunctional adipose tissue. Cancer Epidemiol Biomarkers Prev 2009;18:2569–78.10.1158/1055-9965.EPI-09-0372Search in Google Scholar PubMed

17. Pischon T, Nothlings U, Boeing H. Obesity and cancer. Proc Nutr Soc 2008;67:128–45.10.1017/S0029665108006976Search in Google Scholar PubMed

18. Lichtman MA. Obesity and the risk for a hematological malignancy: leukemia, lymphoma, or myeloma. Oncologist 2010;15:1083–101.10.1634/theoncologist.2010-0206Search in Google Scholar PubMed PubMed Central

19. Dalamaga M, Karmaniolas K, Panagiotou A, Hsi A, Chamberland J, Dimas C, Lekka A, Mantzoros CS. Low circulating adiponectin and resistin, but not leptin, levels are associated with multiple myeloma risk: a case-control study. Cancer Causes Control 2009;20:193–9.10.1007/s10552-008-9233-7Search in Google Scholar PubMed

20. Dalamaga M, Crotty BH, Fargnoli J, Papadavid E, Lekka A, Triantafilli M, Karmaniolas K, Migdalis I, Dionyssiou-Asteriou A, Mantzoros CS. B-cell chronic lymphocytic leukemia risk in association with serum leptin and adiponectin: a case-control study in Greece. Cancer Causes Control 2010;21:1451–9.10.1007/s10552-010-9573-ySearch in Google Scholar PubMed PubMed Central

21. Dalamaga M, Karmaniolas K, Chamberland J, Nikolaidou A, Lekka A, Dionyssiou-Asteriou A, Mantzoros CS. Higher fetuin-A, lower adiponectin and free leptin levels mediate effects of excess body weight on insulin resistance and risk for myelodysplastic syndrome. Metabolism 2013;62:1830–9.10.1016/j.metabol.2013.09.007Search in Google Scholar PubMed

22. Ross JA, Parker E, Blair CK, Cerhan JR, Folsom AR. Body mass index and risk of leukemia in older women. Cancer Epidemiol Biomarkers Prev 2004;13:1810–3.10.1158/1055-9965.EPI-03-2135Search in Google Scholar

23. Larsson SC, Wolk A. Overweight and obesity and incidence of leukemia: a meta-analysis of cohort studies. Int J Cancer 2008;122:1418–21.10.1002/ijc.23176Search in Google Scholar PubMed

24. Wallin A, Larsson SC. Body mass index and risk of multiple myeloma: a meta-analysis of prospective studies. Eur J Cancer 2011;47:1606–15.10.1016/j.ejca.2011.01.020Search in Google Scholar PubMed

25. Chiu BC, Gapstur SM, Greenland P, Wang R, Dyer A. Body mass index, abnormal glucose metabolism, and mortality from hematopoietic cancer. Cancer Epidemiol Biomarkers Prev 2006;15:2348–54.10.1158/1055-9965.EPI-06-0007Search in Google Scholar PubMed

26. Johrer K, Ploner C, Thangavadivel S, Wuggenig P, Greil R. Adipocyte-derived players in hematologic tumors: useful novel targets? Expert Opin Biol Ther 2015;15:61–77.10.1517/14712598.2015.970632Search in Google Scholar PubMed

27. Dalamaga M, Chou SH, Shields K, Papageorgiou P, Polyzos SA, Mantzoros CS. Leptin at the intersection of neuroendocrinology and metabolism: current evidence and therapeutic perspectives. Cell Metab 2013;18:29–42.10.1016/j.cmet.2013.05.010Search in Google Scholar PubMed

28. Moon HS, Dalamaga M, Kim SY, Polyzos SA, Hamnvik OP, Magkos F, Paruthi J, Mantzoros CS. Leptin’s role in lipodystrophic and nonlipodystrophic insulin-resistant and diabetic individuals. Endocr Rev 2013;34:377–412.10.1210/er.2012-1053Search in Google Scholar PubMed PubMed Central

29. Park J, Euhus DM, Scherer PE. Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr Rev 2011;32:550–70.10.1210/er.2010-0030Search in Google Scholar PubMed PubMed Central

30. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 1995;270:26746–9.10.1074/jbc.270.45.26746Search in Google Scholar PubMed

31. Ziemke F, Mantzoros CS. Adiponectin in insulin resistance: lessons from translational research. Am J Clin Nutr 2010;91:258s–61.10.3945/ajcn.2009.28449CSearch in Google Scholar PubMed PubMed Central

32. Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochem Biophys Res Commun 1996;221:286–9.10.1006/bbrc.1996.0587Search in Google Scholar

33. Hu E, Liang P, Spiegelman BM. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 1996;271:10697–703.10.1074/jbc.271.18.10697Search in Google Scholar

34. Nakano Y, Tobe T, Choi-Miura NH, Mazda T, Tomita M. Isolation and characterization of GBP28, a novel gelatin-binding protein purified from human plasma. J Biochem 1996;120:803–12.10.1093/oxfordjournals.jbchem.a021483Search in Google Scholar

35. Takahashi M, Arita Y, Yamagata K, Matsukawa Y, Okutomi K, Horie M, Shimomura I, Hotta K, Kuriyama H, Kihara S, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y. Genomic structure and mutations in adipose-specific gene, adiponectin. Int J Obes Relat Metab Disord 2000;24:861–8.10.1038/sj.ijo.0801244Search in Google Scholar

36. Kaklamani VG, Sadim M, Hsi A, Offit K, Oddoux C, Ostrer H, Ahsan H, Pasche B, Mantzoros C. Variants of the adiponectin and adiponectin receptor 1 genes and breast cancer risk. Cancer Res 2008;68:3178–84.10.1158/0008-5472.CAN-08-0533Search in Google Scholar

37. Shapiro L, Scherer PE. The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr Biol 1998;8:335–8.10.1016/S0960-9822(98)70133-2Search in Google Scholar

38. Hebbard L, Ranscht B. Multifaceted roles of adiponectin in cancer. Best Pract Res Clin Endocrinol Metab 2014;28:59–69.10.1016/j.beem.2013.11.005Search in Google Scholar PubMed PubMed Central

39. Chandran M, Phillips SA, Ciaraldi T, Henry RR. Adiponectin: more than just another fat cell hormone? Diabetes Care 2003;26:2442–50.10.2337/diacare.26.8.2442Search in Google Scholar PubMed

40. Pajvani UB, Du X, Combs TP, Berg AH, Rajala MW, Schulthess T, Engel J, Brownlee M, Scherer PE. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J Biol Chem 2003;278:9073–85.10.1074/jbc.M207198200Search in Google Scholar PubMed

41. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003;423:762–9.10.1038/nature01705Search in Google Scholar PubMed

42. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev 2005;26:439–51.10.1210/er.2005-0005Search in Google Scholar PubMed

43. Kim AY, Lee YS, Kim KH, Lee JH, Lee HK, Jang SH, Kim SE, Lee GY, Lee JW, Jung SA, Chung HY, Jeong S, Kim JB. Adiponectin represses colon cancer cell proliferation via AdipoR1- and -R2-mediated AMPK activation. Mol Endocrinol 2010;24:1441–52.10.1210/me.2009-0498Search in Google Scholar PubMed PubMed Central

44. Hug C, Wang J, Ahmad NS, Bogan JS, Tsao TS, Lodish HF. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Natl Acad Sci USA 2004;101:10308–13.10.1073/pnas.0403382101Search in Google Scholar PubMed PubMed Central

45. Parker-Duffen JL, Nakamura K, Silver M, Kikuchi R, Tigges U, Yoshida S, Denzel MS, Ranscht B, Walsh K. T-cadherin is essential for adiponectin-mediated revascularization. J Biol Chem 2013;288:24886–97.10.1074/jbc.M113.454835Search in Google Scholar PubMed PubMed Central

46. Hebbard LW, Garlatti M, Young LJ, Cardiff RD, Oshima RG, Ranscht B. T-cadherin supports angiogenesis and adiponectin association with the vasculature in a mouse mammary tumor model. Cancer Res 2008;68:1407–16.10.1158/0008-5472.CAN-07-2953Search in Google Scholar PubMed PubMed Central

47. Ouchi N, Kihara S, Arita Y, Okamoto Y, Maeda K, Kuriyama H, Hotta K, Nishida M, Takahashi M, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y. Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway. Circulation 2000;102:1296–301.10.1161/01.CIR.102.11.1296Search in Google Scholar

48. Bluher M, Bullen JW, Jr., Lee JH, Kralisch S, Fasshauer M, Kloting N, Niebauer J, Schon MR, Williams CJ, Mantzoros CS. Circulating adiponectin and expression of adiponectin receptors in human skeletal muscle: associations with metabolic parameters and insulin resistance and regulation by physical training. J Clin Endocrinol Metab 2006;91:2310–6.10.1210/jc.2005-2556Search in Google Scholar PubMed

49. Barb D, Williams CJ, Neuwirth AK, Mantzoros CS. Adiponectin in relation to malignancies: a review of existing basic research and clinical evidence. Am J Clin Nutr 2007;86:s858–66.10.1093/ajcn/86.3.858SSearch in Google Scholar PubMed

50. Hada Y, Yamauchi T, Waki H, Tsuchida A, Hara K, Yago H, Miyazaki O, Ebinuma H, Kadowaki T. Selective purification and characterization of adiponectin multimer species from human plasma. Biochem Biophys Res Commun 2007;356:487–93.10.1016/j.bbrc.2007.03.004Search in Google Scholar PubMed

51. Fabian CJ. Adiponectin: a risk biomarker and attractive target for chemoprevention. J Clin Oncol 2012;30:124–6.10.1200/JCO.2011.38.5500Search in Google Scholar PubMed

52. Yamamoto Y, Hirose H, Saito I, Tomita M, Taniyama M, Matsubara K, Okazaki Y, Ishii T, Nishikai K, Saruta T. Correlation of the adipocyte-derived protein adiponectin with insulin resistance index and serum high-density lipoprotein-cholesterol, independent of body mass index, in the Japanese population. Clin Sci (Lond) 2002;103:137–42.10.1042/CS20010336Search in Google Scholar

53. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, Tataranni PA. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 2001;86:1930–5.10.1210/jcem.86.5.7463Search in Google Scholar PubMed

54. Trujillo ME, Scherer PE. Adiponectin–journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med 2005;257:167–75.10.1111/j.1365-2796.2004.01426.xSearch in Google Scholar PubMed

55. Mazaki-Tovi S, Romero R, Vaisbuch E, Erez O, Mittal P, Chaiworapongsa T, Kim SK, Pacora P, Yeo L, Gotsch F, Dong Z, Yoon BH, Hassan SS, Kusanovic JP. Maternal serum adiponectin multimers in gestational diabetes. J Perinat Med 2009;37:637–50.10.1515/JPM.2009.101Search in Google Scholar PubMed PubMed Central

56. Kishida K, Funahashi T, Shimomura I. Adiponectin as a routine clinical biomarker. Best Pract Res Clin Endocrinol Metab 2014;28:119–30.10.1016/j.beem.2013.08.006Search in Google Scholar PubMed

57. DiMascio L, Voermans C, Uqoezwa M, Duncan A, Lu D, Wu J, Sankar U, Reya T. Identification of adiponectin as a novel hemopoietic stem cell growth factor. J Immunol 2007;178: 3511–20.10.4049/jimmunol.178.6.3511Search in Google Scholar PubMed

58. Yokota T, Meka CS, Kouro T, Medina KL, Igarashi H, Takahashi M, Oritani K, Funahashi T, Tomiyama Y, Matsuzawa Y, Kincade PW. Adiponectin, a fat cell product, influences the earliest lymphocyte precursors in bone marrow cultures by activation of the cyclooxygenase-prostaglandin pathway in stromal cells. J Immunol 2003;171:5091–9.10.4049/jimmunol.171.10.5091Search in Google Scholar PubMed

59. Iversen PO, Wiig H. Tumor necrosis factor alpha and adiponectin in bone marrow interstitial fluid from patients with acute myeloid leukemia inhibit normal hematopoiesis. Clin Cancer Res 2005;11:6793–9.10.1158/1078-0432.CCR-05-1033Search in Google Scholar PubMed

60. Crawford LJ, Peake R, Price S, Morris TC, Irvine AE. Adiponectin is produced by lymphocytes and is a negative regulator of granulopoiesis. J Leukoc Biol 2010;88:807–11.10.1189/jlb.1109723Search in Google Scholar PubMed

61. Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH, Davis KE, Bikman BT, Halberg N, Rutkowski JM, Wade MR, Tenorio VM, Kuo MS, Brozinick JT, Zhang BB, Birnbaum MJ, Summers SA, Scherer PE. Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med 2011;17:55–63.10.1038/nm.2277Search in Google Scholar PubMed PubMed Central

62. Landskroner-Eiger S, Qian B, Muise ES, Nawrocki AR, Berger JP, Fine EJ, Koba W, Deng Y, Pollard JW, Scherer PE. Proangiogenic contribution of adiponectin toward mammary tumor growth in vivo. Clin Cancer Res 2009;15:3265–76.10.1158/1078-0432.CCR-08-2649Search in Google Scholar PubMed PubMed Central

63. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 2004;279:1304–9.10.1074/jbc.M310389200Search in Google Scholar PubMed PubMed Central

64. Brakenhielm E, Veitonmaki N, Cao R, Kihara S, Matsuzawa Y, Zhivotovsky B, Funahashi T, Cao Y. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc Natl Acad Sci USA 2004;101:2476–81.10.1073/pnas.0308671100Search in Google Scholar PubMed PubMed Central

65. Mantzoros C, Petridou E, Dessypris N, Chavelas C, Dalamaga M, Alexe DM, Papadiamantis Y, Markopoulos C, Spanos E, Chrousos G, Trichopoulos D. Adiponectin and breast cancer risk. J Clin Endocrinol Metab 2004;89:1102–7.10.1210/jc.2003-031804Search in Google Scholar PubMed

66. Dalamaga M, Karmaniolas K, Papadavid E, Pelekanos N, Sotiropoulos G, Lekka A. Elevated serum visfatin/nicotinamide phosphoribosyl-transferase levels are associated with risk of postmenopausal breast cancer independently from adiponectin, leptin, and anthropometric and metabolic parameters. Menopause 2011;18:1198–204.10.1097/gme.0b013e31821e21f5Search in Google Scholar PubMed

67. Ishikawa M, Kitayama J, Kazama S, Hiramatsu T, Hatano K, Nagawa H. Plasma adiponectin and gastric cancer. Clin Cancer Res 2005;11:466–72.10.1158/1078-0432.466.11.2Search in Google Scholar

68. Yildirim A, Bilici M, Cayir K, Yanmaz V, Yildirim S, Tekin SB. Serum adiponectin levels in patients with esophageal cancer. Jpn J Clin Oncol 2009;39:92–6.10.1093/jjco/hyn143Search in Google Scholar PubMed

69. Otake S, Takeda H, Suzuki Y, Fukui T, Watanabe S, Ishihama K, Saito T, Togashi H, Nakamura T, Matsuzawa Y, Kawata S. Association of visceral fat accumulation and plasma adiponectin with colorectal adenoma: evidence for participation of insulin resistance. Clin Cancer Res 2005;11:3642–6.10.1158/1078-0432.CCR-04-1868Search in Google Scholar PubMed

70. Strom SS, Yamamura Y, Kantarijian HM, Cortes-Franco JE. Obesity, weight gain, and risk of chronic myeloid leukemia. Cancer Epidemiol Biomarkers Prev 2009;18:1501–6.10.1158/1055-9965.EPI-09-0028Search in Google Scholar PubMed PubMed Central

71. Willett EV, Skibola CF, Adamson P, Skibola DR, Morgan GJ, Smith MT, Roman E. Non-Hodgkin’s lymphoma, obesity and energy homeostasis polymorphisms. Br J Cancer 2005;93: 811–6.10.1038/sj.bjc.6602762Search in Google Scholar PubMed PubMed Central

72. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348:1625–38.10.1056/NEJMoa021423Search in Google Scholar PubMed

73. Lichtman MA. Battling the hematological malignancies: the 200 years’ war. Oncologist 2008;13:126–38.10.1634/theoncologist.2007-0228Search in Google Scholar PubMed

74. Petridou E, Mantzoros CS, Dessypris N, Dikalioti SK, Trichopoulos D. Adiponectin in relation to childhood myeloblastic leukaemia. Br J Cancer 2006;94:156–60.10.1038/sj.bjc.6602896Search in Google Scholar PubMed PubMed Central

75. Aref S, Ibrahim L, Azmy E, Al Ashary R. Impact of serum adiponectin and leptin levels in acute leukemia. Hematology 2013;18:198–203.10.1179/1607845412Y.0000000059Search in Google Scholar PubMed

76. Dalamaga M, Nikolaidou A, Karmaniolas K, Hsi A, Chamberland J, Dionyssiou-Asteriou A, Mantzoros CS. Circulating adiponectin and leptin in relation to myelodysplastic syndrome: a case-control study. Oncology 2007;73:26–32.10.1159/000120995Search in Google Scholar PubMed

77. Dalamaga M, Karmaniolas K, Nikolaidou A, Chamberland J, Hsi A, Dionyssiou-Asteriou A, Mantzoros CS. Adiponectin and resistin are associated with risk for myelodysplastic syndrome, independently from the insulin-like growth factor-I (IGF-I) system. Eur J Cancer 2008;44:1744–53.10.1016/j.ejca.2008.04.015Search in Google Scholar PubMed

78. Avcu F, Ural AU, Yilmaz MI, Bingol N, Nevruz O, Caglar K. Association of plasma adiponectin concentrations with chronic lymphocytic leukemia and myeloproliferative diseases. Int J Hematol 2006;83:254–8.10.1532/IJH97.NA0411Search in Google Scholar PubMed

79. Fitter S, Vandyke K, Schultz CG, White D, Hughes TP, Zannettino AC. Plasma adiponectin levels are markedly elevated in imatinib-treated chronic myeloid leukemia (CML) patients: a mechanism for improved insulin sensitivity in type 2 diabetic CML patients? J Clin Endocrinol Metab 2010;95:3763–7.10.1210/jc.2010-0086Search in Google Scholar PubMed

80. Bouronikou E, Georgoulias P, Giannakoulas N, Valotassiou V, Palassopoulou M, Vassilopoulos G, Papadoulis N, Matsouka P. Metabolism-related cytokine and hormone levels in the serum of patients with myelodysplastic syndromes. Acta Haematol 2013;130:27–33.10.1159/000345427Search in Google Scholar PubMed

81. Reseland JE, Reppe S, Olstad OK, Hjorth-Hansen H, Brenne AT, Syversen U, Waage A, Iversen PO. Abnormal adipokine levels and leptin-induced changes in gene expression profiles in multiple myeloma. Eur J Haematol 2009;83:460–70.10.1111/j.1600-0609.2009.01311.xSearch in Google Scholar PubMed

82. Fowler JA, Lwin ST, Drake MT, Edwards JR, Kyle RA, Mundy GR, Edwards CM. Host-derived adiponectin is tumor-suppressive and a novel therapeutic target for multiple myeloma and the associated bone disease. Blood 2011;118:5872–82.10.1182/blood-2011-01-330407Search in Google Scholar PubMed PubMed Central

83. Hofmann JN, Liao LM, Pollak MN, Wang Y, Pfeiffer RM, Baris D, Andreotti G, Lan Q, Landgren O, Rothman N, Purdue MP. A prospective study of circulating adipokine levels and risk of multiple myeloma. Blood 2012;120:4418–20.10.1182/blood-2012-06-438606Search in Google Scholar PubMed PubMed Central

84. Pamuk GE, Turgut B, Demir M, Vural O. Increased adiponectin level in non-Hodgkin lymphoma and its relationship with interleukin-10. Correlation with clinical features and outcome. J Exp Clin Cancer Res 2006;25:537–41.Search in Google Scholar

85. Moschovi M, Trimis G, Vounatsou M, Katsibardi K, Margeli A, Damianos A, Chrousos G, Papassotiriou I. Serial plasma concentrations of adiponectin, leptin, and resistin during therapy in children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol 2010;32:e8–13.10.1097/MPH.0b013e3181b8a50cSearch in Google Scholar PubMed

86. Kohler JA, Moon RJ, Wright S, Willows E, Davies JH. Increased adiposity and altered adipocyte function in female survivors of childhood acute lymphoblastic leukaemia treated without cranial radiation. Horm Res Paediatr 2011;75:433–40.10.1159/000324412Search in Google Scholar PubMed

87. El-Baz HA, Mosa TE, Elabd EM, Ramadan A, Elharoun AS, Elmorsy EA, Fouda MI. Serum adiponectin and resistin levels in de novo and relapsed acute lymphoblastic leukemia children patients. Iran J Public Health 2013;42:504–10.Search in Google Scholar

88. Esbenshade AJ, Simmons JH, Koyama T, Lindell RB, Friedman DL. Obesity and insulin resistance in pediatric acute lymphoblastic leukemia worsens during maintenance therapy. Pediatr Blood Cancer 2013;60:1287–91.10.1002/pbc.24489Search in Google Scholar PubMed PubMed Central

89. Petridou ET, Dessypris N, Panagopoulou P, Sergentanis TN, Mentis AF, Pourtsidis A, Polychronopoulou S, Kalmanti M, Athanasiadou-Piperopoulou F, Moschovi M. Adipocytokines in relation to Hodgkin lymphoma in children. Pediatr Blood Cancer 2010;54:311–5.10.1002/pbc.22294Search in Google Scholar

90. Petridou ET, Sergentanis TN, Dessypris N, Vlachantoni IT, Tseleni-Balafouta S, Pourtsidis A, Moschovi M, Polychronopoulou S, Athanasiadou-Piperopoulou F, Kalmanti M, Mantzoros CS. Serum adiponectin as a predictor of childhood non-Hodgkin’s lymphoma: a nationwide case-control study. J Clin Oncol 2009;27:5049–55.10.1200/JCO.2008.19.7525Search in Google Scholar PubMed PubMed Central

91. Conroy SM, Maskarinec G, Morimoto Y, Franke AA, Cooney RV, Wilkens LR, Goodman MT, Hernadez BY, Le Marchand L, Henderson BE, Kolonel LN. Non-hodgkin lymphoma and circulating markers of inflammation and adiposity in a nested case-control study: the multiethnic cohort. Cancer Epidemiol Biomarkers Prev 2013;22:337–47.10.1158/1055-9965.EPI-12-0947Search in Google Scholar PubMed PubMed Central

92. Yokota T, Oritani K, Takahashi I, Ishikawa J, Matsuyama A, Ouchi N, Kihara S, Funahashi T, Tenner AJ, Tomiyama Y, Matsuzawa Y. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 2000;96:1723–32.10.1182/blood.V96.5.1723Search in Google Scholar

93. Ozturk K, Avcu F, Ural AU. Aberrant expressions of leptin and adiponectin receptor isoforms in chronic myeloid leukemia patients. Cytokine 2012;57:61–7.10.1016/j.cyto.2011.10.004Search in Google Scholar PubMed

94. Otvos L Jr, Knappe D, Hoffmann R, Kovalszky I, Olah J, Hewitson TD, Stawikowska R, Stawikowski M, Cudic P, Lin F, Wade JD, Surmacz E, Lovas S. Development of second generation peptides modulating cellular adiponectin receptor responses. Front Chem 2014;2:93.10.3389/fchem.2014.00093Search in Google Scholar

95. Wu S, Zheng C, Chen S, Lin B, Chen Y, Zhou W, Li Z. Adiponectin signals through Adiponectin Receptor 1 to reverse imatinib resistance in K562 human chronic myeloid leukemia cells. Biochem Biophys Res Commun 2015;456: 367–72.10.1016/j.bbrc.2014.11.089Search in Google Scholar PubMed

96. Fitter S, Vandyke K, Gronthos S, Zannettino AC. Suppression of PDGF-induced PI3 kinase activity by imatinib promotes adipogenesis and adiponectin secretion. J Mol Endocrinol 2012;48:229–40.10.1530/JME-12-0003Search in Google Scholar PubMed

97. Han S, Jeong AL, Lee S, Park JS, Kim KD, Choi I, Yoon SR, Lee MS, Lim JS, Han SH, Yoon do Y, Yang Y. Adiponectin deficiency suppresses lymphoma growth in mice by modulating NK cells, CD8 T cells, and myeloid-derived suppressor cells. J Immunol 2013;190:4877–86.10.4049/jimmunol.1202487Search in Google Scholar PubMed

98. Willett EV, Morton LM, Hartge P, Becker N, Bernstein L, Boffetta P, Bracci P, Cerhan J, Chiu BC, Cocco P, Dal Maso L, Davis S, De Sanjose S, Smedby KE, Ennas MG, Foretova L, Holly EA, La Vecchia C, Matsuo K, Maynadie M, Melbye M, Negri E, Nieters A, Severson R, Slager SL, Spinelli JJ, Staines A, Talamini R, Vornanen M, Weisenburger DD, Roman E. Non-Hodgkin lymphoma and obesity: a pooled analysis from the InterLymph Consortium. Int J Cancer 2008;122:2062–70.10.1002/ijc.23344Search in Google Scholar PubMed PubMed Central

99. Vendrame E, Martinez-Maza O. Assessment of pre- diagnosis biomarkers of immune activation and inflammation: insights on the etiology of lymphoma. J Proteome Res 2011;10:113–9.10.1021/pr100729zSearch in Google Scholar PubMed PubMed Central

100. Lam QL, Wang S, Ko OK, Kincade PW, Lu L. Leptin signaling maintains B-cell homeostasis via induction of Bcl-2 and Cyclin D1. Proc Natl Acad Sci USA 2010;107:13812–7.10.1073/pnas.1004185107Search in Google Scholar PubMed PubMed Central

101. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004;323:630–5.10.1016/j.bbrc.2004.08.145Search in Google Scholar PubMed

102. Molica S, Vitelli G, Cutrona G, Todoerti K, Mirabelli R, Digiesi G, Giannarelli D, Sperduti I, Molica M, Gentile M, Morabito F, Neri A, Ferrarini M. Prognostic relevance of serum levels and cellular expression of adiponectin in B-cell chronic lymphocytic leukemia. Int J Hematol 2008;88:374–80.10.1007/s12185-008-0165-5Search in Google Scholar PubMed

103. Molica S, Digiesi G, Vacca A, Mirabelli R, Todoerti K, Battaglia C, Morabito F, Neri A, Ribatti D. Does adiponectin act as an antiangiogenic factor in B-cell chronic lymphocytic leukemia? Adv Hematol 2009;2009:287974.10.1155/2009/287974Search in Google Scholar PubMed PubMed Central

104. Lauta VM. A review of the cytokine network in multiple myeloma: diagnostic, prognostic, and therapeutic implications. Cancer 2003;97:2440–52.10.1002/cncr.11072Search in Google Scholar PubMed

105. Ajuwon KM, Spurlock ME. Adiponectin inhibits LPS-induced NF-kappaB activation and IL-6 production and increases PPARgamma2 expression in adipocytes. Am J Physiol Regul Integr Comp Physiol 2005;288:R1220–5.10.1152/ajpregu.00397.2004Search in Google Scholar PubMed

106. Klein B, Tarte K, Jourdan M, Mathouk K, Moreaux J, Jourdan E, Legouffe E, De Vos J, Rossi JF. Survival and proliferation factors of normal and malignant plasma cells. Int J Hematol 2003;78:106–13.10.1007/BF02983377Search in Google Scholar PubMed PubMed Central

107. Dhodapkar MV. Adipokines in MM: time to trim the fat. Blood 2011;118:5716–7.10.1182/blood-2011-10-379834Search in Google Scholar PubMed

108. Medina EA, Oberheu K, Polusani SR, Ortega V, Velagaleti GV, Oyajobi BO. PKA/AMPK signaling in relation to adiponectin’s antiproliferative effect on multiple myeloma cells. Leukemia 2014;28:2080–9.10.1038/leu.2014.112Search in Google Scholar PubMed

109. Peterson SJ, Drummond G, Kim DH, Li M, Kruger AL, Ikehara S, Abraham NG. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice. J Lipid Res 2008;49:1658–69.10.1194/jlr.M800046-JLR200Search in Google Scholar PubMed PubMed Central

110. Drake M, Ng A, Kumar S, Charatcharoenwitthaya Ν, Achenbach S, Holets M, McCready L, Rajkumar SV, Kyle R. Increases in serum levels of dickkopf 1 are associated with alterations in skeletal microstructure in monoclonal gammopathy of undetermined significance [abstract]. The 31st Annual Meeting of the American Society for Bone and Mineral Research, 2009.Search in Google Scholar

Received: 2015-4-6
Accepted: 2015-5-6
Published Online: 2015-6-9
Published in Print: 2015-7-1

©2015 by De Gruyter

Downloaded on 31.5.2024 from https://www.degruyter.com/document/doi/10.1515/hmbci-2015-0016/html
Scroll to top button