Role of Adiponectin in Cervical Cancer

Author(s): Dakshinamurthy Soumya, Dakshinamurthy Swetha, Saimila Momin, Racherla Rishi Gowtham, Egamurthy Dakshinamurthy, Talisetty Bharathi, Divi Venkata Ramana Sai Gopal*

Journal Name: Current Drug Metabolism

Volume 20 , Issue 13 , 2019


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: Cervical Cancer (CC) is the most common leading cancer in women globally. This is considered to be the type of cancer that is restricted to women. Any women in the reproductive age range can develop CC. However, women between the ages of 25 and 39 are at a higher risk.

Objective: In comparison with developed countries, the screening and awareness of CC in developing countries are significantly low. Infection with Human papillomavirus (HPV) is the main cause of CC, especially HPV-16 and HPV-18. Other than HPV, there are other factors that can contribute to CC, such as Human simplex virus (HSV) infection and immunocompromised patients with HIV.

Conclusion: Cervical cancer can be detected by molecular techniques such as (1) PCR, (2) visual acetic acid method, (3) DNA Hybrid II test, (4) liquid-based cytology, (5) Pap-Smear techniques, and (6) colposcopy techniques. Early detection of CC is very much needed; cryotherapy or LEEP (Loop electro surgical excision procedure) can be conducted during the pre-invasive stage of CC. Some metabolic changes in the human body such as fluctuating levels of insulin and triglycerides and increased activity of adiponectin may lead to CC. These contributing factors, such as adipokines, can be used as biomarkers for CC detection.

Keywords: Adiponectin, ADPN, receptors, signaling, growth, Human papillomavirus, HPV, cervical cancer.

[1]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin.,, 2019, 69(1), 7-34.
[http://dx.doi.org/10.3322/caac.21551 ] [PMID: 30620402]
[2]
Ulmer, H.; Bjørge, T.; Concin, H.; Lukanova, A.; Manjer, J.; Hallmans, G.; Borena, W.; Häggström, C.; Engeland, A.; Almquist, M.; Jonsson, H.; Selmer, R.; Stattin, P.; Tretli, S.; Kleiner, A.; Stocks, T.; Nagel, G. Metabolic risk factors and cervical cancer in the metabolic syndrome and cancer project (Me-Can). Gynecol. Oncol., 2012, 125(2), 330-335.
[http://dx.doi.org/10.1016/j.ygyno.2012.01.052] [PMID: 22330614]
[3]
Gelsomino, L.; Naimo, G.D.; Catalano, S.; Mauro, L.; Andò, S. The emerging role of adiponectin in female malignancies. Int. J. Mol. Sci., 2019, 20(9), 2127.
[http://dx.doi.org/10.3390/ijms20092127] [PMID: 31052147]
[4]
Scherer, P.E.; Williams, S.; Fogliano, M.; Baldini, G.; Lodish, H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem., 1995, 270(45), 26746-26749.
[http://dx.doi.org/10.1074/jbc.270.45.26746] [PMID: 7592907]
[5]
Hu, E.; Liang, P.; Spiegelman, B.M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem., 1996, 271(18), 10697-10703.
[http://dx.doi.org/10.1074/jbc.271.18.10697] [PMID: 8631877]
[6]
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(2), 286-289.
[http://dx.doi.org/10.1006/bbrc.1996.0587] [PMID: 8619847]
[7]
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, N.H.; 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(6941), 762-769.
[http://dx.doi.org/10.1038/nature01705] [PMID: 12802337]
[8]
Kadowaki, T.; Yamauchi, T.; Kubota, N. The physiological and pathophysiological role of adiponectin and adiponectin receptors in the peripheral tissues and CNS. FEBS Lett., 2008, 582(1), 74-80.
[http://dx.doi.org/10.1016/j.febslet.2007.11.070] [PMID: 18054335]
[9]
Mantzoros, C.; Petridou, E.; Dessypris, N.; Chavelas, C.; Dalamaga, M.; Alexe, D.M.; Papadiamantis, Y.; Markopoulos, C.; Spanos, E.; Chrousos, G.; Trichopoulos, D. Adiponectin and breast cancer risk. J. Clin. Endocrinol. Metab., 2004, 89(3), 1102-1107.
[http://dx.doi.org/10.1210/jc.2003-031804] [PMID: 15001594]
[10]
Chen, T-H.; Chen, L.; Hsieh, M-S.; Chang, C-P.; Chou, D-T.; Tsai, S-H. Evidence for a protective role for adiponectin in osteoarthritis. Biochim. Biophys. Acta, 2006, 1762, 711-718.
[http://dx.doi.org/10.1016/j.bbadis.2006.06.008]
[11]
Takemura, Y.; Osuga, Y.; Harada, M.; Hirata, T.; Koga, K.; Morimoto, C.; Hirota, Y.; Yoshino, O.; Yano, T.; Taketani, Y. Serum adiponectin concentrations are decreased in women with endometriosis. Hum. Reprod., 2005, 20(12), 3510-3513.
[http://dx.doi.org/10.1093/humrep/dei233] [PMID: 16055459]
[12]
Cust, A.E.; Kaaks, R.; Friedenreich, C.; Bonnet, F.; Laville, M.; Lukanova, A.; Rinaldi, S.; Dossus, L.; Slimani, N.; Lundin, E.; Tjønneland, A.; Olsen, A.; Overvad, K.; Clavel-Chapelon, F.; Mesrine, S.; Joulin, V.; Linseisen, J.; Rohrmann, S.; Pischon, T.; Boeing, H.; Trichopoulos, D.; Trichopoulou, A.; Benetou, V.; Palli, D.; Berrino, F.; Tumino, R.; Sacerdote, C.; Mattiello, A.; Quirós, J.R.; Mendez, M.A.; Sánchez, M.J.; Larrañaga, N.; Tormo, M.J.; Ardanaz, E.; Bueno-de-Mesquita, H.B.; Peeters, P.H.; van Gils, C.H.; Khaw, K.T.; Bingham, S.; Allen, N.; Key, T.; Jenab, M.; Riboli, E. Plasma adiponectin levels and endometrial cancer risk in pre- and postmenopausal women. J. Clin. Endocrinol. Metab., 2007, 92(1), 255-263.
[http://dx.doi.org/10.1210/jc.2006-1371] [PMID: 17062769]
[13]
Sher, D.J.; Oh, W.K.; Jacobus, S.; Regan, M.M.; Lee, G.S.; Mantzoros, C. Relationship between serum adiponectin and prostate cancer grade. Prostate, 2008, 68(14), 1592-1598.
[http://dx.doi.org/10.1002/pros.20823] [PMID: 18646046]
[14]
Otake, S.; Takeda, H.; Fujishima, S.; Fukui, T.; Orii, T.; Sato, T.; Sasaki, Y.; Nishise, S.; Kawata, S. Decreased levels of plasma adiponectin associated with increased risk of colorectal cancer. World J. Gastroenterol., 2010, 16(10), 1252-1257.
[http://dx.doi.org/10.3748/wjg.v16.i10.1252] [PMID: 20222170]
[15]
Ishikawa, M.; Kitayama, J.; Kazama, S.; Hiramatsu, T.; Hatano, K.; Nagawa, H. Plasma adiponectin and gastric cancer. Clin. Cancer Res., 2005, 11(2 Pt 1), 466-472.
[PMID: 15701829]
[16]
Nakano, Y.; Tobe, T.; Choi-Miura, N-H.; Mazda, T.; Tomita, M. Isolation and characterization of GBP28, a novel gelatin-binding protein purified from human plasma. J. Biochem., 1996, 120(4), 803-812.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021483] [PMID: 8947845]
[17]
Khabour, O.F.; Alomari, M.A.; Abu Obaid, A.A. The Relationship of adiponectin level and ADIPOQ gene variants with BMI among young adult women. Dermatoendocrinol, 2018, 10(1)e1477902
[http://dx.doi.org/10.1080/19381980.2018.1477902] [PMID: 30574262]
[18]
Pollin, T.I.; Tanner, K.; O’connell, J.R.; Ott, S.H.; Damcott, C.M.; Shuldiner, A.R.; McLenithan, J.C.; Mitchell, B.D. Linkage of plasma adiponectin levels to 3q27 explained by association with variation in the APM1 gene. Diabetes, 2005, 54(1), 268-274.
[http://dx.doi.org/10.2337/diabetes.54.1.268] [PMID: 15616038]
[19]
Fajas, L.; Fruchart, J-C.; Auwerx, J. Transcriptional control of adipogenesis. Curr. Opin. Cell Biol., 1998, 10(2), 165-173.
[http://dx.doi.org/10.1016/S0955-0674(98)80138-5] [PMID: 9561840]
[20]
Osborne, T.F. Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J. Biol. Chem., 2000, 275(42), 32379-32382.
[http://dx.doi.org/10.1074/jbc.R000017200] [PMID: 10934219]
[21]
Motoshima, H.; Wu, X.; Sinha, M.K.; Hardy, V.E.; Rosato, E.L.; Barbot, D.J.; Rosato, F.E.; Goldstein, B.J. Differential regulation of adiponectin secretion from cultured human omental and subcutaneous adipocytes: effects of insulin and rosiglitazone. J. Clin. Endocrinol. Metab., 2002, 87(12), 5662-5667.
[http://dx.doi.org/10.1210/jc.2002-020635] [PMID: 12466369]
[22]
Yilmaz, M.I.; Sonmez, A.; Caglar, K.; Gok, D.E.; Eyileten, T.; Yenicesu, M.; Acikel, C.; Bingol, N.; Kilic, S.; Oguz, Y.; Vural, A. Peroxisome proliferator-activated receptor γ (PPAR-γ) agonist increases plasma adiponectin levels in type 2 diabetic patients with proteinuria. Endocrine, 2004, 25(3), 207-214.
[http://dx.doi.org/10.1385/ENDO:25:3:207] [PMID: 15758247]
[23]
Doran, A.C.; Meller, N.; Cutchins, A.; Deliri, H.; Slayton, R.P.; Oldham, S.N.; Kim, J.B.; Keller, S.R.; McNamara, C.A. The helix-loop-helix factors Id3 and E47 are novel regulators of adiponectin. Circ. Res., 2008, 103(6), 624-634.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.175893] [PMID: 18669923]
[24]
Jiang, X.; Li, J.; Paskind, M.; Epstein, P.M. Inhibition of calmodulin-dependent phosphodiesterase induces apoptosis in human leukemic cells. Proc. Natl. Acad. Sci. USA, 1996, 93(20), 11236-11241.
[http://dx.doi.org/10.1073/pnas.93.20.11236] [PMID: 8855339]
[25]
Nagaraju, G.P.; Rajitha, B.; Aliya, S.; Kotipatruni, R.P.; Madanraj, A.S.; Hammond, A.; Park, D.; Chigurupati, S.; Alam, A.; Pattnaik, S. The role of adiponectin in obesity-associated female-specific carcinogenesis. Cytokine Growth Factor Rev., 2016, 31, 37-48.
[http://dx.doi.org/10.1016/j.cytogfr.2016.03.014] [PMID: 27079372]
[26]
Kelesidis, I.; Kelesidis, T.; Mantzoros, C.S. Adiponectin and cancer: a systematic review. Br. J. Cancer, 2006, 94(9), 1221-1225.
[http://dx.doi.org/10.1038/sj.bjc.6603051] [PMID: 16570048]
[27]
Balsan, G.A.; Vieira, J.L.C.; Oliveira, A.M.; Portal, V.L. Relationship between adiponectin, obesity and insulin resistance. Rev Assoc Med Bras (1992),, 2015, 61(1), 72-80.
[http://dx.doi.org/10.1590/1806-9282.61.01.072] [PMID: 25909213]
[28]
Hug, C.; Wang, J.; Ahmad, N.S.; Bogan, J.S.; Tsao, T-S.; Lodish, H.F. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. USA, 2004, 101(28), 10308-10313.
[http://dx.doi.org/10.1073/pnas.0403382101] [PMID: 15210937]
[29]
Hebbard, L.W.; Garlatti, M.; Young, L.J.; Cardiff, R.D.; Oshima, R.G.; Ranscht, B. T-cadherin supports angiogenesis and adiponectin association with the vasculature in a mouse mammary tumor model. Cancer Res., 2008, 68(5), 1407-1416.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-2953] [PMID: 18316604]
[30]
Körner, A.; Pazaitou-Panayiotou, K.; Kelesidis, T.; Kelesidis, I.; Williams, C.J.; Kaprara, A.; Bullen, J.; Neuwirth, A.; Tseleni, S.; Mitsiades, N.; Kiess, W.; Mantzoros, C.S. Total and high-molecular-weight adiponectin in breast cancer: in vitro and in vivo studies. J. Clin. Endocrinol. Metab., 2007, 92(3), 1041-1048.
[http://dx.doi.org/10.1210/jc.2006-1858] [PMID: 17192291]
[31]
Palin, M-F.; Bordignon, V.V.; Murphy, B.D. Adiponectin and the control of female reproductive functions. Vitam. Horm., 2012, 90, 239-287.
[32]
Yamauchi, T.; Nio, Y.; Maki, T.; Kobayashi, M.; Takazawa, T.; Iwabu, M.; Okada-Iwabu, M.; Kawamoto, S.; Kubota, N.; Kubota, T.; Ito, Y.; Kamon, J.; Tsuchida, A.; Kumagai, K.; Kozono, H.; Hada, Y.; Ogata, H.; Tokuyama, K.; Tsunoda, M.; Ide, T.; Murakami, K.; Awazawa, M.; Takamoto, I.; Froguel, P.; Hara, K.; Tobe, K.; Nagai, R.; Ueki, K.; Kadowaki, T. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med., 2007, 13(3), 332-339.
[http://dx.doi.org/10.1038/nm1557] [PMID: 17268472]
[33]
Taliaferro-Smith, L.; Nagalingam, A.; Zhong, D.; Zhou, W.; Saxena, N.K.; Sharma, D. LKB1 is required for adiponectin-mediated modulation of AMPK-S6K axis and inhibition of migration and invasion of breast cancer cells. Oncogene, 2009, 28(29), 2621-2633.
[http://dx.doi.org/10.1038/onc.2009.129] [PMID: 19483724]
[34]
Miyoshi, Y.; Funahashi, T.; Kihara, S.; Taguchi, T.; Tamaki, Y.; Matsuzawa, Y.; Noguchi, S. Association of serum adiponectin levels with breast cancer risk. Clin. Cancer Res., 2003, 9(15), 5699-5704.
[PMID: 14654554]
[35]
Dal Maso, L.; Augustin, L.S.; Franceschi, S.; Talamini, R.; Polesel, J.; Kendall, C.W.; Jenkins, D.J.; Vidgen, E.; La Vecchia, C. Association between components of the insulin-like growth factor system and epithelial ovarian cancer risk. Oncology, 2004, 67(3-4), 225-230.
[http://dx.doi.org/10.1159/000081322] [PMID: 15557783]
[36]
Goktas, S.; Yilmaz, M.I.; Caglar, K.; Sonmez, A.; Kilic, S.; Bedir, S. Prostate cancer and adiponectin. Urology, 2005, 65(6), 1168-1172.
[http://dx.doi.org/10.1016/j.urology.2004.12.053] [PMID: 15922427]
[37]
Yokota, T.; Oritani, K.; Takahashi, I.; Ishikawa, J.; Matsuyama, A.; Ouchi, N.; Kihara, S.; Funahashi, T.; Tenner, A.J.; 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(5), 1723-1732.
[http://dx.doi.org/10.1182/blood.V96.5.1723] [PMID: 10961870]
[38]
Arita, Y.; Kihara, S.; Ouchi, N.; Maeda, K.; Kuriyama, H.; Okamoto, Y.; Kumada, M.; Hotta, K.; Nishida, M.; Takahashi, M.; Nakamura, T.; Shimomura, I.; Muraguchi, M.; Ohmoto, Y.; Funahashi, T.; Matsuzawa, Y. Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation, 2002, 105(24), 2893-2898.
[http://dx.doi.org/10.1161/01.CIR.0000018622.84402.FF] [PMID: 12070119]
[39]
Wang, C.; Xin, X.; Xiang, R.; Ramos, F.J.; Liu, M.; Lee, H.J.; Chen, H.; Mao, X.; Kikani, C.K.; Liu, F.; Dong, L.Q. Yin-Yang regulation of adiponectin signaling by APPL isoforms in muscle cells. J. Biol. Chem., 2009, 284(46), 31608-31615.
[http://dx.doi.org/10.1074/jbc.M109.010355] [PMID: 19661063]
[40]
Bråkenhielm, E.; Veitonmäki, 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(8), 2476-2481.
[http://dx.doi.org/10.1073/pnas.0308671100] [PMID: 14983034]
[41]
Lacey, J.V., Jr; Swanson, C.A.; Brinton, L.A.; Altekruse, S.F.; Barnes, W.A.; Gravitt, P.E.; Greenberg, M.D.; Hadjimichael, O.C.; McGowan, L.; Mortel, R.; Schwartz, P.E.; Kurman, R.J.; Hildesheim, A. Obesity as a potential risk factor for adenocarcinomas and squamous cell carcinomas of the uterine cervix. Cancer, 2003, 98(4), 814-821.
[http://dx.doi.org/10.1002/cncr.11567] [PMID: 12910527]
[42]
Dal Maso, L.; Augustin, L.S.; Karalis, A.; Talamini, R.; Franceschi, S.; Trichopoulos, D.; Mantzoros, C.S.; La Vecchia, C. Circulating adiponectin and endometrial cancer risk. J. Clin. Endocrinol. Metab., 2004, 89(3), 1160-1163.
[http://dx.doi.org/10.1210/jc.2003-031716] [PMID: 15001602]
[43]
Tsuchida, A.; Yamauchi, T.; Takekawa, S.; Hada, Y.; Ito, Y.; Maki, T.; Kadowaki, T. Peroxisome proliferator-activated receptor (PPAR)α activation increases adiponectin receptors and reduces obesity-related inflammation in adipose tissue: comparison of activation of PPARalpha, PPARgamma, and their combination. Diabetes, 2005, 54(12), 3358-3370.
[http://dx.doi.org/10.2337/diabetes.54.12.3358] [PMID: 16306350]
[44]
Liu, J.-L.; Cui, W.; Li, B.; Lu, Y. Possible roles of reg family proteins in pancreatic islet cell growth, Endocrine, Metabolic & Immune Disorders-Drug Targets (Formerly Current Drug Targets-Immune, Endocrine & Metabolic Disorders) 2008, 8, 1-10.
[45]
Li, H.; Stampfer, M.J.; Mucci, L.; Rifai, N.; Qiu, W.; Kurth, T.; Ma, J. A 25-year prospective study of plasma adiponectin and leptin concentrations and prostate cancer risk and survival. Clin. Chem., 2010, 56(1), 34-43.
[http://dx.doi.org/10.1373/clinchem.2009.133272] [PMID: 19910504]
[46]
Tao, L.; Wang, Y.; Gao, E.; Zhang, H.; Yuan, Y.; Lau, W.B.; Chan, L.; Koch, W.J.; Ma, X.L. Adiponectin: an indispensable molecule in rosiglitazone cardioprotection following myocardial infarction. Circ. Res., 2010, 106(2), 409-417.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.211797] [PMID: 19940263]
[47]
Zhou, L.; Deepa, S.S.; Etzler, J.C.; Ryu, J.; Mao, X.; Fang, Q.; Liu, D.D.; Torres, J.M.; Jia, W.; Lechleiter, J.D.; Liu, F.; Dong, L.Q. Adiponectin activates AMP-activated protein kinase in muscle cells via APPL1/LKB1-dependent and phospholipase C/Ca2+/Ca2+/ calmodulin-dependent protein kinase kinase-dependent pathways. J. Biol. Chem., 2009, 284(33), 22426-22435.
[http://dx.doi.org/10.1074/jbc.M109.028357] [PMID: 19520843]
[48]
Wang, Y.; Lam, K.S.; Yau, M.H.; Xu, A. Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem. J., 2008, 409(3), 623-633.
[http://dx.doi.org/10.1042/BJ20071492] [PMID: 18177270]
[49]
Simpson, F.; Whitehead, J.P. Adiponectin-it’s all about the modifications. Int. J. Biochem. Cell Biol., 2010, 42(6), 785-788.
[http://dx.doi.org/10.1016/j.biocel.2009.12.021] [PMID: 20044026]
[50]
Waki, H.; Yamauchi, T.; Kamon, J.; Ito, Y.; Uchida, S.; Kita, S.; Hara, K.; Hada, Y.; Vasseur, F.; Froguel, P.; Kimura, S.; Nagai, R.; Kadowaki, T. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem., 2003, 278(41), 40352-40363.
[http://dx.doi.org/10.1074/jbc.M300365200] [PMID: 12878598]
[51]
Tsao, T-S.; Tomas, E.; Murrey, H.E.; Hug, C.; Lee, D.H.; Ruderman, N.B.; Heuser, J.E.; Lodish, H.F. Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J. Biol. Chem., 2003, 278(50), 50810-50817.
[http://dx.doi.org/10.1074/jbc.M309469200] [PMID: 14522956]
[52]
Wang, Y.; Xu, A.; Knight, C.; Xu, L.Y.; Cooper, G.J. Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J. Biol. Chem., 2002, 277(22), 19521-19529.
[http://dx.doi.org/10.1074/jbc.M200601200] [PMID: 11912203]
[53]
Wang, Y.; Lam, K.S.; Chan, L.; Chan, K.W.; Lam, J.B.; Lam, M.C.; Hoo, R.C.; Mak, W.W.; Cooper, G.J.; Xu, A. Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J. Biol. Chem., 2006, 281(24), 16391-16400.
[http://dx.doi.org/10.1074/jbc.M513907200] [PMID: 16621799]
[54]
Anelli, T.; Alessio, M.; Bachi, A.; Bergamelli, L.; Bertoli, G.; Camerini, S.; Mezghrani, A.; Ruffato, E.; Simmen, T.; Sitia, R. Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J., 2003, 22(19), 5015-5022.
[http://dx.doi.org/10.1093/emboj/cdg491] [PMID: 14517240]
[55]
Wang, Z.V.; Schraw, T.D.; Kim, J-Y.; Khan, T.; Rajala, M.W.; Follenzi, A.; Scherer, P.E. Secretion of the adipocyte-specific secretory protein adiponectin critically depends on thiol-mediated protein retention. Mol. Cell. Biol., 2007, 27(10), 3716-3731.
[http://dx.doi.org/10.1128/MCB.00931-06] [PMID: 17353260]
[56]
Schraw, T.; Wang, Z.V.; Halberg, N.; Hawkins, M.; Scherer, P.E. Plasma adiponectin complexes have distinct biochemical characteristics. Endocrinology, 2008, 149(5), 2270-2282.
[http://dx.doi.org/10.1210/en.2007-1561] [PMID: 18202126]
[57]
Buechler, C.; Wanninger, J.; Neumeier, M. Adiponectin receptor binding proteins--recent advances in elucidating adiponectin signalling pathways. FEBS Lett., 2010, 584(20), 4280-4286.
[http://dx.doi.org/10.1016/j.febslet.2010.09.035] [PMID: 20875820]
[58]
Heiker, J.T.; Kosel, D.; Beck-Sickinger, A.G. Molecular mechanisms of signal transduction via adiponectin and adiponectin receptors. Biol. Chem., 2010, 391(9), 1005-1018.
[http://dx.doi.org/10.1515/bc.2010.104] [PMID: 20536390]
[59]
Mao, X.; Kikani, C.K.; Riojas, R.A.; Langlais, P.; Wang, L.; Ramos, F.J.; Fang, Q.; Christ-Roberts, C.Y.; Hong, J.Y.; Kim, R-Y.; Liu, F.; Dong, L.Q. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol., 2006, 8(5), 516-523.
[http://dx.doi.org/10.1038/ncb1404] [PMID: 16622416]
[60]
Heiker, J.T.; Wottawah, C.M.; Juhl, C.; Kosel, D.; Mörl, K.; Beck-Sickinger, A.G. Protein kinase CK2 interacts with adiponectin receptor 1 and participates in adiponectin signaling. Cell. Signal., 2009, 21(6), 936-942.
[http://dx.doi.org/10.1016/j.cellsig.2009.02.003] [PMID: 19233263]
[61]
Xu, Y.; Wang, N.; Ling, F.; Li, P.; Gao, Y. Receptor for activated C-kinase 1, a novel binding partner of adiponectin receptor 1. Biochem. Biophys. Res. Commun., 2009, 378(1), 95-98.
[http://dx.doi.org/10.1016/j.bbrc.2008.11.026] [PMID: 19010305]
[62]
Charlton, H.K.; Webster, J.; Kruger, S.; Simpson, F.; Richards, A.A.; Whitehead, J.P. ERp46 binds to AdipoR1, but not AdipoR2, and modulates adiponectin signalling. Biochem. Biophys. Res. Commun., 2010, 392(2), 234-239.
[http://dx.doi.org/10.1016/j.bbrc.2010.01.029] [PMID: 20074551]
[63]
Kobayashi, H.; Ouchi, N.; Kihara, S.; Walsh, K.; Kumada, M.; Abe, Y.; Funahashi, T.; Matsuzawa, Y. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ. Res., 2004, 94(4), e27-e31.
[http://dx.doi.org/10.1161/01.RES.0000119921.86460.37] [PMID: 14752031]
[64]
Cheng, K.K.; Lam, K.S.; Wang, Y.; Huang, Y.; Carling, D.; Wu, D.; Wong, C.; Xu, A. Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPL1 in endothelial cells. Diabetes, 2007, 56(5), 1387-1394.
[http://dx.doi.org/10.2337/db06-1580] [PMID: 17287464]
[65]
Cheng, K.K.; Iglesias, M.A.; Lam, K.S.; Wang, Y.; Sweeney, G.; Zhu, W.; Vanhoutte, P.M.; Kraegen, E.W.; Xu, A. APPL1 potentiates insulin-mediated inhibition of hepatic glucose production and alleviates diabetes via Akt activation in mice. Cell Metab., 2009, 9(5), 417-427.
[http://dx.doi.org/10.1016/j.cmet.2009.03.013] [PMID: 19416712]
[66]
Chandrasekar, B.; Boylston, W.H.; Venkatachalam, K.; Webster, N.J.; Prabhu, S.D.; Valente, A.J. Adiponectin blocks interleukin-18-mediated endothelial cell death via APPL1-dependent AMP-activated protein kinase (AMPK) activation and IKK/NF-kappaB/PTEN suppression. J. Biol. Chem., 2008, 283(36), 24889-24898.
[http://dx.doi.org/10.1074/jbc.M804236200] [PMID: 18632660]
[67]
Cleasby, M.E.; Lau, Q.; Polkinghorne, E.; Patel, S.A.; Leslie, S.J.; Turner, N.; Cooney, G.J.; Xu, A.; Kraegen, E.W. The adaptor protein APPL1 increases glycogen accumulation in rat skeletal muscle through activation of the PI3-kinase signalling pathway. J. Endocrinol., 2011, 210(1), 81-92.
[http://dx.doi.org/10.1530/JOE-11-0039] [PMID: 21543456]
[68]
Xin, X.; Zhou, L.; Reyes, C.M.; Liu, F.; Dong, L.Q. APPL1 mediates adiponectin-stimulated p38 MAPK activation by scaffolding the TAK1-MKK3-p38 MAPK pathway. Am. J. Physiol. Endocrinol. Metab., 2011, 300(1), E103-E110.
[http://dx.doi.org/10.1152/ajpendo.00427.2010] [PMID: 20978232]
[69]
Arita, Y.; Kihara, S.; Ouchi, N.; Takahashi, M.; Maeda, K.; Miyagawa, J.; Hotta, K.; Shimomura, I.; Nakamura, T.; Miyaoka, K.; Kuriyama, H.; Nishida, M.; Yamashita, S.; Okubo, K.; Matsubara, K.; Muraguchi, M.; Ohmoto, Y.; Funahashi, T.; Matsuzawa, Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun., 1999, 257(1), 79-83.
[http://dx.doi.org/10.1006/bbrc.1999.0255] [PMID: 10092513]
[70]
Ouchi, N.; Kihara, S.; Funahashi, T.; Matsuzawa, Y.; Walsh, K. Obesity, adiponectin and vascular inflammatory disease. Curr. Opin. Lipidol., 2003, 14(6), 561-566.
[http://dx.doi.org/10.1097/00041433-200312000-00003] [PMID: 14624132]
[71]
Spranger, J.; Kroke, A.; Möhlig, M.; Bergmann, M.M.; Ristow, M.; Boeing, H.; Pfeiffer, A.F. Adiponectin and protection against type 2 diabetes mellitus. Lancet, 2003, 361(9353), 226-228.
[http://dx.doi.org/10.1016/S0140-6736(03)12255-6] [PMID: 12547549]
[72]
Ryo, M.; Nakamura, T.; Kihara, S.; Kumada, M.; Shibazaki, S.; Takahashi, M.; Nagai, M.; Matsuzawa, Y.; Funahashi, T. Adiponectin as a biomarker of the metabolic syndrome. Circ. J., 2004, 68(11), 975-981.
[http://dx.doi.org/10.1253/circj.68.975] [PMID: 15502375]
[73]
Liu, Z.; Liu, J.; Jahn, L.A.; Fowler, D.E.; Barrett, E.J. Infusing lipid raises plasma free fatty acids and induces insulin resistance in muscle microvasculature. J. Clin. Endocrinol. Metab., 2009, 94(9), 3543-3549.
[http://dx.doi.org/10.1210/jc.2009-0027] [PMID: 19567533]
[74]
Maruthur, N.M.; Bolen, S.D.; Brancati, F.L.; Clark, J.M. The association of obesity and cervical cancer screening: a systematic review and meta-analysis. Obesity (Silver Spring), 2009, 17(2), 375-381.
[http://dx.doi.org/10.1038/oby.2008.480] [PMID: 18997682]
[75]
Xie, L.; Wang, Y.; Wang, S.; Wu, N.; Chen, Y.; Yan, J. Adiponectin induces growth inhibition and apoptosis in cervical cancer HeLa cells. Biologia, 2011, 66, 712-720.
[http://dx.doi.org/10.2478/s11756-011-0063-9]
[76]
Combs, T.P.; Berg, A.H.; Rajala, M.W.; Klebanov, S.; Iyengar, P.; Jimenez-Chillaron, J.C.; Patti, M.E.; Klein, S.L.; Weinstein, R.S.; Scherer, P.E. Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes, 2003, 52(2), 268-276.
[http://dx.doi.org/10.2337/diabetes.52.2.268] [PMID: 12540596]
[77]
Cnop, M.; Havel, P.J.; Utzschneider, K.M.; Carr, D.B.; Sinha, M.K.; Boyko, E.J.; Retzlaff, B.M.; Knopp, R.H.; Brunzell, J.D.; Kahn, S.E. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia, 2003, 46(4), 459-469.
[http://dx.doi.org/10.1007/s00125-003-1074-z] [PMID: 12687327]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 13
Year: 2019
Published on: 23 January, 2020
Page: [1033 - 1038]
Pages: 6
DOI: 10.2174/1389200221666200103113330
Price: $65

Article Metrics

PDF: 24
HTML: 3
EPUB: 1
PRC: 1