Adiponectin: Potential Protein Hormone as a Candidate Biomarker for Male Fertility

H Hafizuddin, Ni Wayan Kurniani Karja, Lisa Praharani, Mohamad Agus Setiadi

Abstract

Reproduction is an important factor that requires attention to increase livestock production. The application of artificial insemination (AI) technology has been developed rapidly in the world, so that availability of fertile superior male is a determinant factor of successful AI. Several recent studies have been aimed to discover male fertility biomarker, by intense research on fertility-associated proteins contained in seminal plasma. This paper describes the role of adiponectin as a biomarker candidate of male fertility. Adiponectin has a positive effect on spermatozoa functionality and steroidogenesis. This has been proven by several studies that found its expression in Sertoli cells and Leydig cells in the reproductive tract. Based on the specific role on spermatozoa functionality and steroidogenesis in supporting male fertility parameter, it is strongly suggested that adiponectin is an excellent candidate biomarker for male fertility.

Keywords

Adiponectin; biomarker; fertility; male; spermatozoa

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References

Abdelrahman SS, Abdalla MSE, Darderi TM, Ali EAE. 2018. Association of body weight, scrotal circumference, heart girth and penile development with spermatogenesis in the Nubian bucks. J Vet Med Anim Health. 10:217-223.

Achari A, Jain S. 2017. Adiponectin, a therapeutic target for obesity, diabetes, and endothelial dysfunction. Int J Mol Sci. 18:1-17.

Agga GE, Udala U, Regassa F, Wudie A. 2011. Body measurements of bucks of three goat breeds in Ethiopia and their correlation to breed, age and testicular measurements. Small Rumin Res. 95:133-138.

Azamar-Llamas D, Hernández-Molina G, Ramos-Ávalos B, Furuzawa-Carballeda J. 2017. Adipokine contribution to the pathogenesis of osteoarthritis. Mediat Inflamm. 2017:1-26.

Bertoldo M, Faure M, Dupont J, Froment P. 2015. AMPK: a master energy regulator for gonadal function. Front Neurosci. 9:1-11.

Boe-Hansen GB, Rego JPA, Crisp JM, Moura AA, Nouwens AS, Li Y, Venus B, Burns BM, McGowan MR. 2015. Seminal plasma proteins and their relationship with percentage of morphologically normal sperm in 2-year-old Brahman (Bos indicus) bulls. Anim Reprod Sci. 162:20-30.

Caballero I, Parrilla I, Almiñana C, del Olmo D, Roca J, Martínez E, Vázquez J. 2012. Seminal plasma proteins as modulators of the sperm function and their application in sperm biotechnologies. Reprod Domest Anim. 47:12-21.

Campos DB, Palin MF, Bordignon V, Murphy BD. 2008. The ‘beneficial’ adipokines in reproduction and fertility. Int J Obes. 32:223-231.

Choubey M, Ranjan A, Bora PS, Baltazar F, Krishna A. 2019. Direct actions of adiponectin on changes in reproductive, metabolic, and anti-oxidative enzymes status in the testis of adult mice. Gen Comp Endocrinol. 279:1-11.

de Abreu VG, Martins CJdM, de Oliveira PAC, Francischetti EA. 2017. High-molecular weight adiponectin/HOMA-IR ratio as a biomarka of metabolic syndrome in urban multiethnic Brazilian subjects. PLoS One. 12:1-12.

de Oliveira RV, Dogan S, Belser LE, Kaya A, Topper E, Moura A, Thibaudeau G, Memili E. 2013. Molecular morphology and function of bull spermatozoa linked to histones and associated with fertility. Reproduction. 146:263-272.

Deepa SS, Dong LQ. 2009. APPL1: role in adiponectin signaling and beyond. Am J Physiol Endocrinol Metab. 296:E22-E36.

Dogan S, Vargovic P, Oliveira R, Belser LE, Kaya A, Moura A, Sutovsky P, Parrish J, Topper E, Memili E. 2015. Sperm protamine-status correlates to the fertility of breeding bulls. Biol Reprod. 92:1-9.

Ebinuma H, Yago H, Akimoto Y, Miyazaki O, Kadowaki T, Yamauchi T, Hara K. 2011. Method of selectively assaying adiponectin multimers. Google Patents.

Elfassy Y, Bastard J-P, McAvoy C, Fellahi S, Dupont J, Levy R. 2018. Adipokines in semen: physiopathology and effects on spermatozoa. Int J Endocrinol. 2018:1-11.

Foote RH. 2003. Fertility estimation: a review of past experience and future prospects. Anim Reprod Sci. 75:119-139.

Galardo MN, Riera MF, Pellizzari EH, Sobarzo C, Scarcelli R, Denduchis B, Lustig L, Cigorraga SB, Meroni SB. 2010. Adenosine regulates Sertoli cell function by activating AMPK. Mol Cell Endocrinol. 330:49-58.

Gregoraszczuk E, Slupecka M, Wolinski J, Hejmej A, Bilinska B, Fiedor E, Piwnicka N, Rak A. 2016. Maternal high-fat diet during pregnancy and lactation had gender difference effect on adiponectin in rat offspring. J Physiol Pharmacol. 67:543-553.

Hada Y, Yamauchi T, Waki H, Tsuchida A, Hara K, Yago H, Miyazaki O, Ebinuma H, Kadowaki T. 2007. Selective purification and characterization of adiponectin multimer species from human plasma. Biochem Biophys Res Commun. 356:487-493.

Hafizuddin H, Karja N, Praharani L, Setiadi M. 2019. Adiponectin and testosterone levels and its correlation with fertility in Anglo-Nubian x Etawah Grade crossbred bucks. Trop Anim Sci J (In Review).

Hedia MG, El-Belely MS, Ismail ST, Abo El-Maaty AM. 2019. Monthly changes in testicular blood flow dynamics and their association with testicular volume, plasma steroid hormones profile and semen characteristics in rams. Theriogenology. 123:68-73.

Heinz JF, Singh SP, Janowitz U, Hoelker M, Tesfaye D, Schellander K, Sauerwein H. 2015. Characterization of adiponectin concentrations and molecular weight forms in serum, seminal plasma, and ovarian follicular fluid from cattle. Theriogenology. 83:326-333.

Hug C, Wang J, Ahmad NS, Bogan JS, Tsao T-S, Lodish HF. 2004. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Nat Acad Sci USA. 101:10308-10313.

Jagir S, Ajeet K, Dhaliwal G. 2010. Pelvic area and scrotal circumference in relation to libido in breeding bulls. Indian Vet J. 87:396-397.

Kadivar A, Khoei HH, Hassanpour H, Golestanfar A, Ghanaei H. 2016. Correlation of adiponectin mRNA abundance and its receptors with quantitative parameters of sperm motility in rams. Int J Fertil Steril. 10:127-135.

Kadowaki T, Yamauchi T. 2005. Adiponectin and adiponectin receptors. Endocr Rev. 26:439-451.

Kasimanickam VR, Kasimanickam RK, Kastelic JP, Stevenson JS. 2013. Associations of adiponectin and fertility estimates in Holstein bulls. Theriogenology. 79:766-777.

Kawwass JF, Summer R, Kallen CB. 2015. Direct effects of leptin and adiponectin on peripheral reproductive tissues: a critical review. Mol Hum Reprod. 21:617-632.

Kaya A, Memili E. 2016. Sperm macromolecules associated with bull fertility. Anim Reprod Sci. 169:88-94.

Liu L-L, Xian H, Cao J-C, Zhang C, Zhang Y-H, Chen M-M, Qian Y, Jiang M. 2015. Peroxisome proliferator-activated receptor gamma signaling in human sperm physiology. Asian J Androl. 17:942-947.

Liu Z, Xiao T, Peng X, Li G, Hu F. 2017. APPLs: More than just adiponectin receptor binding proteins. Cell Signal. 32:76-84.

Mahmood S, Kumar A, Singh R, Sarkar M, Singh G, Verma M, Kumar G. 2018. Scrotal circumference: A predictor of testosterone concentration and certain attributes of seminal vesicles influencing buffalo male fertility. Vet World. 11:739-747.

Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim R-Y et al. 2006. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol. 8:516-523.

Martin LJ. 2014. Implications of adiponectin in linking metabolism to testicular function. Endocrine. 46:16-28.

Menzies‐Gow N, Knowles E, Rogers I, Rendle D. 2019. Validity and application of immunoturbidimetric and enzyme‐linked immunosorbent assays for the measurement of adiponectin concentration in ponies. Equine Vet J. 51:33-37.

Michalakis KG, Segars JH. 2010. The role of adiponectin in reproduction: from polycystic ovary syndrome to assisted reproduction. Fertil Steril. 94:1949-1957.

Mielenz M, Mielenz B, Singh SP, Kopp C, Heinz J, Häussler S, Sauerwein H. 2013. Development, validation, and pilot application of a semiquantitative Western blot analysis and an ELISA for bovine adiponectin. Domest Anim Endocrin. 44:121-130.

Moradi M, Doustimotlagh AH, Dehpour AR, Rahimi N, Golestani A. 2019. The influence of TRAIL, adiponectin and sclerostin alterations on bone loss in BDL-induced cirrhotic rats and the effect of opioid system blockade. Life Sci. 233:116706.

Mousavi MS, Shahverdi A, Drevet J, Akbarinejad V, Esmaeili V, Sayahpour FA, Topraggaleh TR, Rahimizadeh P, Alizadeh A. 2019. Peroxisome Proliferator-Activated Receptors (PPARs) levels in spermatozoa of normozoospermic and asthenozoospermic men. Syst Biol Reprod Med. 2019:1-11.

Naseer Z, Ahmad E, Aksoy M. 2014. Cholesterol efflux from sperm: approaches and applications. Turk J Vet Anim Sci. 38:653-659.

Ouedraogo R, Wu X, Xu S-Q, Fuchsel L, Motoshima H, Mahadev K, Hough K, Scalia R, Goldstein BJ. 2006. Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes. 55:1840-1846.

Pardo M, Roca-Rivada A, Seoane LM, Casanueva FF. 2012. Obesidomics: contribution of adipose tissue secretome analysis to obesity research. Endocrine. 41:374-383.

Parker R, Mathis C, Hawkins D. 1999. Evaluating the breeding soundness of beef bulls. Washington (USA): Cooperative Extension Service, College of Agriculture and Home Economics Washington State University. p. 1-4.

Pearson L. 2015. Adiponectin in equine reproduction. Washington (USA): Washington State University.

Petherick JC. 2005. A review of some factors affecting the expression of libido in beef cattle, and individual bull and herd fertility. Appl Anim Behav Sci. 90:185-205.

Pfaehler A, Nanjappa MK, Coleman ES, Mansour M, Wanders D, Plaisance EP, Judd RL, Akingbemi BT. 2012. Regulation of adiponectin secretion by soy isoflavones has implication for endocrine function of the testis. Toxicol Lett. 209:78-85.

Rahmanifar F, Tabandeh MR. 2012. Adiponectin and its receptors gene expression in the reproductive tract of ram. Small Rumin Res. 105:263-267.

Rak A, Mellouk N, Froment P, Dupont J. 2017. Adiponectin and resistin: potential metabolic signals affecting hypothalamo-pituitary gonadal axis in females and males of different species. Reproduction. 153:R215-R226.

Ramachandran R, Maddineni S, Ocón-Grove O, Hendricks III G, Vasilatos-Younken R, Hadley JA. 2013. Expression of adiponectin and its receptors in avian species. Gen Comp Endocrinol. 190:88-95.

Ranjan A. 2017. Adipokines as a modulator of reproductive function. J Sci Res. 61:131-140.

Rato L, Alves MG, Socorro S, Duarte AI, Cavaco JE, Oliveira PF. 2012. Metabolic regulation is important for spermatogenesis. Nat Rev Urol. 9:330-338.

Rodrigues M, Souza C, Martins J, Rego J, Oliveira J, Domont G, Nogueira F, Moura A. 2013. Seminal plasma proteins and their relationship with sperm motility in Santa Ines rams. Small Rumin Res. 109:94-100.

Rodríguez-Martínez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ. 2011. Seminal plasma proteins: what role do they play?. Am J Reprod Immunol. 66:11-22.

Rodriguez-Pacheco F, Martinez-Fuentes AJ, Tovar S, Pinilla L, Tena-Sempere M, Dieguez C, Castano JP, Malagon MM. 2007. Regulation of pituitary cell function by adiponectin. Endocrinology. 148:401-410.

Santoro M, Guido C, De Amicis F, Sisci D, Vizza D, Gervasi S, Carpino A, Aquila S. 2013. Sperm metabolism in pigs: a role for peroxisome proliferator-activated receptor gamma (PPARγ). J Exp Biol. 216:1085-1092.

Sarlós P, Egerszegi I, Balogh O, Molnár A, Cseh S, Rátky J. 2013. Seasonal changes of scrotal circumference, blood plasma testosterone concentration and semen characteristics in Racka rams. Small Rumin Res. 111:90-95.

Shupe J, Cheng J, Puri P, Kostereva N, Walker WH. 2011. Regulation of Sertoli-Germ cell adhesion and sperm release by FSH and nonclassical testosterone signaling. Mol Endocrinol. 25:238-252.

Singh A, Brar P, Cheema R. 2014. Relationships among frozen-thawed semen fertility, physical parameters, certain routine sperm characteristics and testosterone in breeding Murrah buffalo (Bubalus bubalis) bulls. Vet World. 7:644-651.

Sinha MK, Songer T, Xiao Q, Sloan JH, Wang J, Ji S, Alborn WE, Davis RA, Swarbrick MM, Stanhope KL. 2007. Analytical validation and biological evaluation of a high-molecular-weight adiponectin ELISA. Clin Chem. 53:2144-2151.

Smolinska N, Kiezun M, Dobrzyn K, Szeszko K, Maleszka A, Kaminski T. 2017. Adiponectin, orexin A and orexin B concentrations in the serum and uterine luminal fluid during early pregnancy of pigs. Anim Reprod Sci. 178:1-8.

Tanita T, Miyakoshi H, Nakano Y. 2008. Performance of ELISA for specific measurement of high-molecular-weight (HMW) adiponectin. J Immunol Methods. 333:139-146.

Thomas S, Kratzsch D, Schaab M, Scholz M, Grunewald S, Thiery J, Paasch U, Kratzsch J. 2013. Seminal plasma adipokine levels are correlated with functional characteristics of spermatozoa. Fertil Steril. 99:1256-1263.

Tilg H, Wolf AM. 2005. Adiponectin: a key fat-derived molecule regulating inflammation. Expert Opin Ther Targets. 9:245-251.

Tvarijonaviciute A, Martínez-Subiela S, Ceron JJ. 2010. Validation of 2 commercially available enzyme-linked immunosorbent assays for adiponectin determination in canine serum samples. Can J Vet Res. 74:279-285.

Utt MD. 2016. Prediction of bull fertility. Anim Reprod Sci. 169:37-44.

Waite R, Dwyer C, Beggs D, Mansell P, Stevenson M, Pyman M. 2019. Scrotal circumference, bodyweight and semen characteristics in growing dairy-breed natural-service bulls in Tasmania, Australia. New Zeal Vet J. 67:109-116.

Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S, Hara K, Hada Y, Vasseur F, Froguel P et al. 2003. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J Biol Chem. 278:40352-40363.

Wilkinson M, Brown R, Imran SA, Ur E. 2007. Adipokine gene expression in brain and pituitary gland. Neuroendocrinology. 86:191-209.

Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, et al. 2007. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med. 13:332-339.

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