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RESEARCH ARTICLE

Relationships between placental adiponectin, leptin, visfatin and resistin and birthweight in cattle

Liuhong Shen A * , Yingkun Zhu A * , Jinbang Xiao A , Bolin Qian A , Tao Jiang A , Junliang Deng A , Guangneng Peng A , Shumin Yu A , Suizhong Cao https://orcid.org/0000-0003-0741-572X A C , Zhicai Zuo A , Xiaoping Ma A , Zhijun Zhong A , Zhihua Ren A , Ya Wang A , Ziyao Zhou A , Haifeng Liu A , Xiaolan Zong B and Yanchun Hu A
+ Author Affiliations
- Author Affiliations

A Sichuan Agricultural University, Chengdu Campus, The Key Laboratory of Animal Disease and Human Health of Sichuan Province, College of Veterinary Medicine, Chengdu, Sichuan, 611130, China.

B Sichuan Agricultural University, Chengdu Campus, Academic Affairs Office, Chengdu, Sichuan, 611130, China.

C Corresponding author. Email: suizhongcao@sicau.edu.cn

Reproduction, Fertility and Development 32(4) 402-408 https://doi.org/10.1071/RD18247
Submitted: 30 July 2018  Accepted: 1 July 2019   Published: 19 November 2019

Abstract

Adipokines can affect intrauterine development while calf birthweight (CBW) is a breeding standard of calves, which reflects the status of fetal intrauterine development. To explore the correlation between placental adipokines and CBW, 54 healthy Chinese Holstein cows were used in the present study. The cows were grouped according to the CBW of their calves. Placentas were collected immediately after delivery and enzyme-linked immunosorbent assay and reverse transcription-polymerase chain reaction were used to detect the placental expression levels of adiponectin, leptin, visfatin and resistin. Our results show that the mRNA transcription and blood placental content of adiponectin, leptin, visfatin and resistin increased with increasing CBW. The analysis showed that the mRNA transcription levels of placental adiponectin, leptin and resistin were positively correlated with CBW. The mRNA and protein expression levels of adiponectin, leptin and visfatin between the three groups were significantly correlated. Placental resistin mRNA levels correlated positively with adiponectin mRNA, but not leptin or visfatin. The protein expression levels of resistin were significantly positively correlated with those of adiponectin, leptin and visfatin. These results suggest that placental adipokines play important roles in regulating calf intrauterine growth.

Additional keywords: adipokines, calve birth weight, placenta.


References

Arias-Alvarez, M., Bermejo-Alvarez, P., Gutierrez-Adan, A., Rizos, D., Lorenzo, P. L., and Lonergan, P. (2011). Effect of leptin supplementation during in vitro oocyte maturation and embryo culture on bovine embryo development and gene expression patterns. Theriogenology 75, 887–896.
Effect of leptin supplementation during in vitro oocyte maturation and embryo culture on bovine embryo development and gene expression patterns.Crossref | GoogleScholarGoogle Scholar | 21196029PubMed |

Astern, J. M., Collier, A. C., and Kendal-Wright, C. E. (2013). Pre-B cell colony enhancing factor (PBEF/NAMPT/visfatin) and vascular endothelial growth factor (VEGF) cooperate to increase the permeability of the human placental amnion. Placenta 34, 42–49.
Pre-B cell colony enhancing factor (PBEF/NAMPT/visfatin) and vascular endothelial growth factor (VEGF) cooperate to increase the permeability of the human placental amnion.Crossref | GoogleScholarGoogle Scholar | 23151382PubMed |

Aye, I. L., Powell, T. L., and Jansson, T. (2013). Review: adiponectin – the missing link between maternal adiposity, placental transport and fetal growth? Placenta 34, S40–S45.
Review: adiponectin – the missing link between maternal adiposity, placental transport and fetal growth?Crossref | GoogleScholarGoogle Scholar | 23245987PubMed |

Aye, I. L. M. H., Rosario, F. J., Powell, T. L., and Thomas, J. (2015). Adiponectin supplementation in pregnant mice prevents the adverse effects of maternal obesity on placental function and fetal growth. Proc. Natl. Acad. Sci. USA 112, 12858–12863.
Adiponectin supplementation in pregnant mice prevents the adverse effects of maternal obesity on placental function and fetal growth.Crossref | GoogleScholarGoogle Scholar |

Bajoria, R., Sooranna, S. R., Ward, B. S., and Chatterjee, R. (2002). Prospective function of placental leptin at maternal–fetal interface. Placenta 23, 103–115.
Prospective function of placental leptin at maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 11945077PubMed |

Balogh, O., Staub, L. P., Gram, A., Boos, A., Kowalewski, M. P., and Reichler, I. M. (2015). Leptin in the canine uterus and placenta: possible implications in pregnancy. Reprod. Biol. Endocrinol. 13, 13.
Leptin in the canine uterus and placenta: possible implications in pregnancy.Crossref | GoogleScholarGoogle Scholar | 25871422PubMed |

Banerjee, R. R., Rangwala, S. M., Shapiro, J. S., Rich, A. S., Rhoades, B., Qi, Y., Wang, J., Rajala, M. W., Pocai, A., Scherer, P. E., Steppan, C. M., Ahima, R. S., Obici, S., Rossetti, L., and Lazar, M. A. (2004). Regulation of fasted blood glucose by resistin. Science 303, 1195–1198.
Regulation of fasted blood glucose by resistin.Crossref | GoogleScholarGoogle Scholar | 14976316PubMed |

Benaitreau, D., Dos Santos, E., Leneveu, M. C., Alfaidy, N., Feige, J. J., de Mazancourt, P., Pecquery, R., and Dieudonné, M. N. (2010). Effects of adiponectin on human trophoblast invasion. J. Endocrinol. 207, 45–53.
Effects of adiponectin on human trophoblast invasion.Crossref | GoogleScholarGoogle Scholar | 20675305PubMed |

Briana, D. D., and Malamitsi-Puchner, A. (2009). Intrauterine growth restriction and adult disease: the role of adipocytokines. Eur. J. Endocrinol. 160, 337–347.
Intrauterine growth restriction and adult disease: the role of adipocytokines.Crossref | GoogleScholarGoogle Scholar | 19095781PubMed |

Briana, D. D., Liosi, S., Gourgiotis, D., Boutsikou, M., Marmarinos, A., Baka, S., Hassiakos, D., and Malamitsi-Puchner, A. (2012). Fetal concentrations of the growth factors TGF-α and TGF-β1 in relation to normal and restricted fetal growth at term. Cytokine 60, 157–161.
Fetal concentrations of the growth factors TGF-α and TGF-β1 in relation to normal and restricted fetal growth at term.Crossref | GoogleScholarGoogle Scholar | 22732125PubMed |

Caminos, J. E., Nogueiras, R., Gallego, R., Bravo, S., Tovar, S., García-Caballero, T., Casanueva, F. F., and Diéguez, C. (2005). Expression and regulation of adiponectin and receptor in human and rat placenta. J. Clin. Endocrinol. Metab. 90, 4276–4286.
Expression and regulation of adiponectin and receptor in human and rat placenta.Crossref | GoogleScholarGoogle Scholar | 15855268PubMed |

Castellucci, M., De Matteis, R., Meisser, A., Cancello, R., Monsurrò, V., Islami, D., Sarzani, R., Marzioni, D., Cinti, S., and Bischof, P. (2000). Leptin modulates extracellular matrix molecules and metalloproteinases: possible implications for trophoblast invasion. Mol. Hum. Reprod. 6, 951–958.
Leptin modulates extracellular matrix molecules and metalloproteinases: possible implications for trophoblast invasion.Crossref | GoogleScholarGoogle Scholar | 11006325PubMed |

Cho, G. J., Yoo, S. W., Hong, S. C., Oh, M. J., Kim, T., Kim, H. J., Lee, K. W., and Kim, S. H. (2006). Correlations between umbilical and maternal serum resistin levels and neonatal birth weight. Acta Obstet. Gynecol. Scand. 85, 1051–1056.
| 16929409PubMed |

Dawczynski, K., Vries, H. D., Beck, J. F., Wittig, S., Pfaffendorf-Regler, N., Hübler, A., and Schleußner, E. (2012). The relation of adiponectin serum concentration and adiponectin mRNA expression in materno–feto–placental unit in uncomplicated pregnancy. Z. Geburtshilfe Neonatol. 216, 38.
The relation of adiponectin serum concentration and adiponectin mRNA expression in materno–feto–placental unit in uncomplicated pregnancy.Crossref | GoogleScholarGoogle Scholar |

Dos Santos, E., Serazin, V., Morvan, C., Torre, A., Wainer, R., Mazancourt, P. D., and Dieudonné, M. N. (2012). Adiponectin and leptin systems in human endometrium during window of implantation. Fertil. Steril. 97, 771–778.e1.
Adiponectin and leptin systems in human endometrium during window of implantation.Crossref | GoogleScholarGoogle Scholar | 22265003PubMed |

Dos Santos, E., Duval, F., Vialard, F., and Dieudonné, M. N. (2015). The roles of leptin and adiponectin at the fetal–maternal interface in humans. Horm. Mol. Biol. Clin. Investig. 24, 47–63.
The roles of leptin and adiponectin at the fetal–maternal interface in humans.Crossref | GoogleScholarGoogle Scholar | 26509784PubMed |

Farid, S. D., Najati, N., Gharebaghi, M. M., Haghjo, A. G., and Ghojazadeh, M. (2013). Resistin in cord blood of small for gestation age and appropriate for gestation age term neonates. Iran. J. Pediatr. 23, 659.
| 24910744PubMed |

Guzel, S., Seven, A., Guzel, E. C., Buyuk, B., Celebi, A., and Aydemir, B. (2013). Visfatin, leptin, and TNF-α: interrelated adipokines in insulin-resistant clinical and subclinical hypothyroidism. Endocr. Res. 38, 184–194.
Visfatin, leptin, and TNF-α: interrelated adipokines in insulin-resistant clinical and subclinical hypothyroidism.Crossref | GoogleScholarGoogle Scholar | 23324036PubMed |

Herrera, E., and Ortega-Senovilla, H. (2014). Lipid metabolism during pregnancy and its implications for fetal growth. Curr. Pharm. Biotechnol. 15, 24–31.
Lipid metabolism during pregnancy and its implications for fetal growth.Crossref | GoogleScholarGoogle Scholar | 24720597PubMed |

Ikeda, Y., Tsuchiya, H., Hama, S., Kajimoto, K., and Kogure, K. (2013). Resistin affects lipid metabolism during adipocyte maturation of 3T3–L1 cells. FEBS J. 280, 5884–5895.
Resistin affects lipid metabolism during adipocyte maturation of 3T3–L1 cells.Crossref | GoogleScholarGoogle Scholar | 24034627PubMed |

Ikeda, Y., Tsuchiya, H., Hama, S., Kajimoto, K., and Kogure, K. (2014). Resistin regulates the expression of plasminogen activator inhibitor-1 in 3T3–L1 adipocytes. Biochem. Biophys. Res. Commun. 448, 129–133.
Resistin regulates the expression of plasminogen activator inhibitor-1 in 3T3–L1 adipocytes.Crossref | GoogleScholarGoogle Scholar | 24667608PubMed |

Jamali, R., Razavizade, M., Arj, A., and Aarabi, M. H. (2016). Serum adipokines might predict liver histology findings in non-alcoholic fatty liver disease. World J. Gastroenterol. 22, 5096–5103.
Serum adipokines might predict liver histology findings in non-alcoholic fatty liver disease.Crossref | GoogleScholarGoogle Scholar | 27275102PubMed |

Karakosta, P., Chatzi, L., Plana, E., Margioris, A., Castanas, E., and Kogevinas, M. (2011). Leptin levels in cord blood and anthropometric measures at birth: a systematic review and meta-analysis. Paediatr. Perinat. Epidemiol. 25, 150–163.
Leptin levels in cord blood and anthropometric measures at birth: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 21281328PubMed |

Kępczyńska, M. A., Wargent, E. T., Cawthorne, M. A., Arch, J. R., O’Dowd, J. F., and Stocker, C. J. (2013). Circulating levels of the cytokines IL10, IFN-γ and resistin in an obese mouse model of developmental programming. J. Dev. Orig. Health Dis. 4, 491–498.
Circulating levels of the cytokines IL10, IFN-γ and resistin in an obese mouse model of developmental programming.Crossref | GoogleScholarGoogle Scholar | 24924228PubMed |

Kesser, J., Hill, M., Heinz, J. F. L., Koch, C., Rehage, J., Steinhoff-Wagner, J., Hammon, H. M., Mielenz, B., Sauerwein, H., and Sadri, H. (2015). The rapid increase of circulating adiponectin in neonatal calves depends on colostrum intake. J. Dairy Sci. 98, 7044–7051.
The rapid increase of circulating adiponectin in neonatal calves depends on colostrum intake.Crossref | GoogleScholarGoogle Scholar | 26277307PubMed |

Lepercq, J., Cauzac, M., Lahlou, N., Timsit, J., Girard, J., Auwerx, J., and Hauguelde, M. S. (1998). Overexpression of placental leptin in diabetic pregnancy: a critical role for insulin. Diabetes 47, 847–850.
Overexpression of placental leptin in diabetic pregnancy: a critical role for insulin.Crossref | GoogleScholarGoogle Scholar | 9588462PubMed |

Ma, Y., Cheng, Y., Wang, J., Cheng, H., Zhou, S., and Li, X. (2010). The changes of visfatin in serum and its expression in fat and placental tissue in pregnant women with gestational diabetes. Diabetes Res. Clin. Pract. 90, 60–65.
The changes of visfatin in serum and its expression in fat and placental tissue in pregnant women with gestational diabetes.Crossref | GoogleScholarGoogle Scholar | 20621376PubMed |

Maymó, J. L., Pérez, A. P., Gambino, Y., Calvo, J. C., Sánchez-Margalet, V., and Varone, C. L. (2011). Review: leptin gene expression in the placenta – regulation of a key hormone in trophoblast proliferation and survival. Placenta 32, S146–S153.
Review: leptin gene expression in the placenta – regulation of a key hormone in trophoblast proliferation and survival.Crossref | GoogleScholarGoogle Scholar | 21303721PubMed |

Morgan, S. A., Bringolf, J. B., and Seidel, E. R. (2008). Visfatin expression is elevated in normal human pregnancy. Peptides 29, 1382–1389.
Visfatin expression is elevated in normal human pregnancy.Crossref | GoogleScholarGoogle Scholar | 18524416PubMed |

McDonald, E. A., and Wolfe, M. W. (2011). The pro-inflammatory role of adiponectin at the maternal–fetal interface. Am. J. Reprod. Immunol. 66, 128–136.
The pro-inflammatory role of adiponectin at the maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 21244561PubMed |

Mumtaz, S., Alsaif, S., Wray, S., and Noble, K. (2015). Inhibitory effect of visfatin and leptin on human and rat myometrial contractility ☆. Life Sci. 125, 57–62.
Inhibitory effect of visfatin and leptin on human and rat myometrial contractility ☆.Crossref | GoogleScholarGoogle Scholar | 25645057PubMed |

Ogueh, O., Sooranna, S., Nicolaides, K. H., and Johnson, M. R. (2000). The relationship between leptin concentration and bone metabolism in the human fetus. J. Clin. Endocrinol. Metab. 85, 1997–1999.
The relationship between leptin concentration and bone metabolism in the human fetus.Crossref | GoogleScholarGoogle Scholar | 10843187PubMed |

Palanivel, R., and Sweeney, G. (2005). Regulation of fatty acid uptake and metabolism in L6 skeletal muscle cells by resistin. FEBS Lett. 579, 5049–5054.
Regulation of fatty acid uptake and metabolism in L6 skeletal muscle cells by resistin.Crossref | GoogleScholarGoogle Scholar | 16137686PubMed |

Patel, L., Buckels, A. C., Kinghorn, I. J., Murdock, P. R., Holbrook, J. D., Plumpton, C., Macphee, C. H., and Smith, S. A. (2003). Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem. Biophys. Res. Commun. 300, 472–476.
Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators.Crossref | GoogleScholarGoogle Scholar | 12504108PubMed |

Pavlová, T., Novák, J., and Bienertová-Vašků, J. (2015). The role of visfatin (PBEF/Nampt) in pregnancy complications. J. Reprod. Immunol. 112, 102–110.
The role of visfatin (PBEF/Nampt) in pregnancy complications.Crossref | GoogleScholarGoogle Scholar | 26451650PubMed |

Peng, X. D., Xie, H., Zhao, Q., Wu, X. P., Sun, Z. Q., and Liao, E. Y. (2008). Relationships between serum adiponectin, leptin, resistin, visfatin levels and bone mineral density, and bone biochemical markers in Chinese men. Clin. Chim. Acta 387, 31–35.
Relationships between serum adiponectin, leptin, resistin, visfatin levels and bone mineral density, and bone biochemical markers in Chinese men.Crossref | GoogleScholarGoogle Scholar | 17884030PubMed |

Pérez-Pérez, A., Maymó, J., Gambino, Y., Dueñas, J. L., Goberna, R., Varone, C., and Sánchez-Margalet, V. (2009). Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells. Biol. Reprod. 81, 826–832.
Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells.Crossref | GoogleScholarGoogle Scholar | 19553602PubMed |

Rajala, M. W., Ying, L., Mollie, R., Man, Y. X., Hao, Q., Ron, G., Nir, B., and Scherer, P. E. (2002). Cell type-specific expression and coregulation of murine resistin and resistin-like molecule-alpha in adipose tissue. Mol. Endocrinol. 16, 1920.
Cell type-specific expression and coregulation of murine resistin and resistin-like molecule-alpha in adipose tissue.Crossref | GoogleScholarGoogle Scholar | 12145345PubMed |

Reese, J., Das, S., Paria, B., Lim, H., Song, H., Matsumoto, H., Knudtson, K., DuBois, R., and Dey, S. (2001). Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J. Biol. Chem. 276, 44137–44145.
Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation.Crossref | GoogleScholarGoogle Scholar | 11551965PubMed |

Ren, Y., Zuo, Z. C., and Wan, T. M. (2016). Resistin: its role in insulin resistance and mechanism of action. Acta physiologica Sinica 68, 65.
| 26915324PubMed |

Sitticharoon, C., Nway, N. C., Chatree, S., Churintaraphan, M., Boonpuan, P., and Maikaew, P. (2014). Interactions between adiponectin, visfatin, and omentin in subcutaneous and visceral adipose tissues and serum, and correlations with clinical and peripheral metabolic factors. Peptides 62, 164–175.
Interactions between adiponectin, visfatin, and omentin in subcutaneous and visceral adipose tissues and serum, and correlations with clinical and peripheral metabolic factors.Crossref | GoogleScholarGoogle Scholar | 25453978PubMed |

Steppan, C. M., Bailey, S. T., Bhat, S., Brown, E. J., Banerjee, R. R., Wright, C. M., Patel, H. R., Ahima, R. S., and Lazar, M. A. (2001). The hormone resistin links obesity to diabetes. Nature 409, 307–312.
The hormone resistin links obesity to diabetes.Crossref | GoogleScholarGoogle Scholar | 11201732PubMed |

Stock, S. M., and Bremme, K. A. (1998). Elevation of plasma leptin levels during pregnancy in normal and diabetic women ☆. Metabolism 47, 840.
Elevation of plasma leptin levels during pregnancy in normal and diabetic women ☆.Crossref | GoogleScholarGoogle Scholar | 9667232PubMed |

Ta, N., Li, J., Wei, B., and B. L., C. (2010). Study on the relationship of adiponectin in gestational diabetes mellitus rats ‘placenta and birth weight of newborn mouses. Maternal and Child Health Care of China 25, 4121–4125.

Tsai, P. J., Davis, J., Thompson, K., and Bryant-Greenwood, G. (2015). Visfatin/Nampt and SIRT1: roles in post-term delivery in pregnancies associated with obesity. Reprod. Sci. 22, 1028.
Visfatin/Nampt and SIRT1: roles in post-term delivery in pregnancies associated with obesity.Crossref | GoogleScholarGoogle Scholar | 25670718PubMed |

Urrego, T., Vásquez, G. M., and Gómez-Puerta, J. A. (2016). Relationship between obesity, adipokines and systemic lupus erythematosus. Rev. Fac. Cien. Med. Univ. Nac. Cordoba 73, 32.
| 27419894PubMed |

Valsamakis, G., Papatheodorou, D. C., Margeli, A., Bakoulas, V., Kapantais, E., Papassotiriou, I., Creatsas, G., Kumar, S., and Mastorakos, G. (2014). First trimester maternal BMI is a positive predictor of cord blood c-peptide levels while maternal visfatin levels is a negative predictor of birth weight. Hormones (Athens) 13, 87.
First trimester maternal BMI is a positive predictor of cord blood c-peptide levels while maternal visfatin levels is a negative predictor of birth weight.Crossref | GoogleScholarGoogle Scholar | 24722131PubMed |

Wang, J., Shang, L. X., Dong, X., Wang, X., Wu, N., Wang, S. H., Zhang, F., Xu, L. M., and Xiao, Y. (2010). Relationship of adiponectin and resistin levels in umbilical serum, maternal serum and placenta with neonatal birth weight. Aust. N. Z. J. Obstet. Gynaecol. 50, 432–438.
Relationship of adiponectin and resistin levels in umbilical serum, maternal serum and placenta with neonatal birth weight.Crossref | GoogleScholarGoogle Scholar | 21039376PubMed |

Yan, F., Hemin, N., Yunhai, L., Yong, G., Lin, L., and Xueying, L. (2014). Effects of leptin on in vitro early embryonic development diapause. Acta Veterinaria et Zootechnica Sinica. 45, 763–768.

Yoon, S. J., Cha, K. Y., and Lee, K. A. (2005). Leptin receptors are down-regulated in uterine implantation sites compared to interimplantation sites. Mol. Cell. Endocrinol. 232, 27–35.
Leptin receptors are down-regulated in uterine implantation sites compared to interimplantation sites.Crossref | GoogleScholarGoogle Scholar | 15737466PubMed |

Zhang, X., Gao, Y. H., and Zhao, H. Z. (2011). Expressions of leptin and its receptor in placenta and their relationship with newborn infant weight. China Journal of Modern Medicine 21, 1876–1879.
Expressions of leptin and its receptor in placenta and their relationship with newborn infant weight.Crossref | GoogleScholarGoogle Scholar |

Zhong, W. (2015). Detection of visfatin, Xiap and Survivin expressions in placenta tissue of preeclampsia and its correlation with serum indexes. Journal of Hainan Medical University 2015, 105–108.
Detection of visfatin, Xiap and Survivin expressions in placenta tissue of preeclampsia and its correlation with serum indexes.Crossref | GoogleScholarGoogle Scholar |