Increased expression of dermatopontin and its implications for testicular dysfunction in mice

Cai,Jun; Liu,Weijia; Hao,Jie; Chen,Maoxin; Li,Gang

doi:10.3892/mmr.2016.4879

Increased expression of dermatopontin and its implications for testicular dysfunction in mice

Authors:
- Jun Cai
- Weijia Liu
- Jie Hao
- Maoxin Chen
- Gang Li
View Affiliations

Affiliations: Institute of Life Sciences, Chongqing Medical University, Chongqing 400016, P.R. China, Experimental Research Center, The First Affiliated Hospital, Chongqing Medical University, Chongqing 400016, P.R. China
Published online on: February 5, 2016 https://doi.org/10.3892/mmr.2016.4879
Pages: 2431-2438
Copyright: © Cai et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

An array of specific and non‑specific molecules, which are expressed in the testis, have been demonstrated to be responsible for testicular function. Our previous study revealed that dermatopontin (DPT) is expressed in Sertoli cells of the testis, however, its roles in testicular function remains somewhat elusive. In the present study, CdCl2‑ and busulfan‑induced testicular dysfunction models were used to investigate the implications of DPT expression for testicular function. The mRNA and protein expression levels of DPT were detected using reverse transcription‑quantitative polymerase chain reaction and western blotting, respectively. A negative correlation was observed between testicular damage and the expression of DPT, which suggested that an increase in DPT expression may be a marker for testicular dysfunction. This result was corroborated by the finding that transgenic mice exhibiting Sertoli cell‑specific overexpression of DPT exhibited damage to their testicular morphology. Additionally, DPT overexpression in the testis affected the expression levels of claudin‑11 and zonula occludens‑1, which indicated that DPT may affect testicular function by affecting the integrity of the blood‑testis barrier (BTB). In conclusion, the present study provided evidence to suggest that DPT may be indicative of mouse testicular dysfunction, since increased expression may be associated with damage to the BTB.

View Figures

View References

1	Irvine DS: Epidemiology and aetiology of male infertility. Hum Reprod. 13(Suppl 1): 33–44. 1998. View Article : Google Scholar : PubMed/NCBI
2	Gnoth C, Godehardt E, Frank-Herrmann P, Friol K, Tigges J and Freundl G: Definition and prevalence of subfertility and infertility. Hum Reprod. 20:1144–1147. 2005. View Article : Google Scholar : PubMed/NCBI
3	Sepehrimanesh M, Kazemipour N, Saeb M and Nazifi S: Analysis of rat testicular proteome following 30-day exposure to 900 MHz electromagnetic field radiation. Electrophoresis. 35:3331–3338. 2014. View Article : Google Scholar : PubMed/NCBI
4	Fowler PA, Cassie S, Rhind SM, Brewer MJ, Collinson JM, Lea RG, Baker PJ, Bhattacharya S and O'Shaughnessy PJ: Maternal smoking during pregnancy specifically reduces human fetal desert hedgehog gene expression during testis development. J Clin Endocrinol Metab. 93:619–626. 2008. View Article : Google Scholar
5	Thonneau P, Bujan L, Multigner L and Mieusset R: Occupational heat exposure and male fertility: A review. Hum Reprod. 13:2122–2125. 1998. View Article : Google Scholar : PubMed/NCBI
6	Benavides-Garcia R, Joachim R, Pina NA, Mutoji KN, Reilly MA and Hermann BP: Granulocyte colony-stimulating factor prevents loss of spermatogenesis after sterilizing busulfan chemotherapy. Fertil Steril. 103:270.e8–280.e8. 2015. View Article : Google Scholar
7	Spiazzi CC, Manfredini V, Barcellos da Silva FE, Flores EM, Izaguirry AP, Vargas LM, Soares MB and Santos FW: γ-Oryzanol protects against acute cadmium-induced oxidative damage in mice testes. Food Chem Toxicol. 55:526–532. 2013. View Article : Google Scholar : PubMed/NCBI
8	Haouem S, Najjar MF, El Hani A and Sakly R: Accumulation of cadmium and its effects on testis function in rats given diet containing cadmium-polluted radish bulb. Exp Toxicol Pathol. 59:307–311. 2008. View Article : Google Scholar
9	Mabrouk A and Cheikh HB: Thymoquinone supplementation ameliorates lead-induced testis function impairment in adult rats. Toxicol Ind Health. 2014.Epub ahead of print. View Article : Google Scholar : PubMed/NCBI
10	Sharma P, Huq AU and Singh R: Cypermethrin-induced reproductive toxicity in the rat is prevented by resveratrol. J Hum Reprod Sci. 7:99–106. 2014. View Article : Google Scholar : PubMed/NCBI
11	Ismail MF and Mohamed HM: Deltamethrin-induced genotoxicity and testicular injury in rats: Comparison with biopesticide. Food Chem Toxicol. 50:3421–3425. 2012. View Article : Google Scholar : PubMed/NCBI
12	Walczak-Jedrzejowska R, Wolski JK and Slowikowska-Hilczer J: The role of oxidative stress and antioxidants in male fertility. Cent European J Urol. 66:60–67. 2013. View Article : Google Scholar
13	Desai SS, Roy BS and Mahale SD: Mutations and polymorphisms in FSH receptor: Functional implications in human reproduction. Reproduction. 146:R235–R248. 2013. View Article : Google Scholar : PubMed/NCBI
14	Smith LB and Walker WH: The regulation of spermatogenesis by androgens. Semin Cell Dev Biol. 30:2–13. 2014. View Article : Google Scholar : PubMed/NCBI
15	Xiao X, Mruk DD and Cheng CY: Intercellular adhesion molecules (ICAMs) and spermatogenesis. Hum Reprod Update. 19:167–186. 2013. View Article : Google Scholar : PubMed/NCBI
16	Eid N, Ito Y and Otsuki Y: Enhanced mitophagy in Sertoli cells of ethanol-treated rats: Morphological evidence and clinical relevance. J Mol Histol. 43:71–80. 2012. View Article : Google Scholar
17	Li MW, Mruk DD, Lee WM and Cheng CY: Disruption of the blood-testis barrier integrity by bisphenol A in vitro: Is this a suitable model for studying blood-testis barrier dynamics? Int J Biochem Cell Biol. 41:2302–2314. 2009. View Article : Google Scholar : PubMed/NCBI
18	Alam MS, Ohsako S, Tay TW, Tsunekawa N, Kanai Y and Kurohmaru M: Di (n-butyl) phthalate induces vimentin filaments disruption in rat Sertoli cells: A possible relation with spermatogenic cell apoptosis. Anat Histol Embryol. 39:186–193. 2010. View Article : Google Scholar : PubMed/NCBI
19	Zhang X and Lui WY: Dysregulation of nectin-2 in the testicular cells: An explanation of cadmium-induced male infertility. Biochim Biophys Acta. 1839:873–884. 2014. View Article : Google Scholar : PubMed/NCBI
20	Neame PJ, Choi HU and Rosenberg LC: The isolation and primary structure of a 22-kDa extracellular matrix protein from bovine skin. J Biol Chem. 264:5474–5479. 1989.PubMed/NCBI
21	Choi HU, Johnson TL, Pal S, Tang LH, Rosenberg L and Neame PJ: Characterization of the dermatan sulfate proteoglycans, DS-PGI and DS-PGII, from bovine articular cartilage and skin isolated by octyl-sepharose chromatography. J Biol Chem. 264:2876–2884. 1989.PubMed/NCBI
22	Superti-Furga A, Rocchi M, Schäfer BW and Gitzelmann R: Complementary DNA sequence and chromosomal mapping of a human proteoglycan-binding cell-adhesion protein (dermatopontin). Genomics. 17:463–467. 1993. View Article : Google Scholar : PubMed/NCBI
23	Okamoto O, Suzuki Y, Kimura S and Shinkai H: Extracellular matrix 22-kDa protein interacts with decorin core protein and is expressed in cutaneous fibrosis. J Biochem. 119:106–114. 1996. View Article : Google Scholar : PubMed/NCBI
24	Okamoto O, Fujiwara S, Abe M and Sato Y: Dermatopontin interacts with transforming growth factor beta and enhances its biological activity. Biochem J. 337:537–541. 1999. View Article : Google Scholar : PubMed/NCBI
25	Cooper LJ, Bentley AJ, Nieduszynski IA, Talabani S, Thomson A, Utani A, Shinkai H, Fullwood NJ and Brown GM: The role of dermatopontin in the stromal organization of the cornea. Invest Ophthalmol Vis Sci. 47:3303–3310. 2006. View Article : Google Scholar : PubMed/NCBI
26	Takeuchi T, Suzuki M, Kumagai J, Kamijo T, Sakai M and Kitamura T: Extracellular matrix dermatopontin modulates prostate cell growth in vivo. J Endocrinol. 190:351–361. 2006. View Article : Google Scholar : PubMed/NCBI
27	Yang Q, Hao J, Chen M and Li G: Dermatopontin is a novel regulator of the CdCl2-induced decrease in claudin-11 expression. Toxicol In Vitro. 28:1158–1164. 2014. View Article : Google Scholar : PubMed/NCBI
28	Giuili G, Shen WH and Ingraham HA: The nuclear receptor SF-1 mediates sexually dimorphic expression of mullerian inhibiting substance, in vivo. Development. 124:1799–1807. 1997.PubMed/NCBI
29	Jeffs B, Ito M, Yu RN, Martinson FA, Wang ZJ, Doglio LT and Jameson JL: Sertoli cell-specific rescue of fertility, but not testicular pathology, in Dax1 (Ahch)-deficient male mice. Endocrinology. 142:2481–2488. 2001.PubMed/NCBI
30	Narula A, Kilen S, Ma E, Kroeger J, Goldberg E and Woodruff TK: Smad4 overexpression causes germ cell ablation and leydig cell hyperplasia in transgenic mice. Am J Pathol. 161:1723–1734. 2002. View Article : Google Scholar : PubMed/NCBI
31	Zohni K, Zhang X, Tan SL, Chan P and Nagano MC: The efficiency of male fertility restoration is dependent on the recovery kinetics of spermatogonial stem cells after cytotoxic treatment with busulfan in mice. Hum Reprod. 27:44–53. 2012. View Article : Google Scholar
32	Kanatsu-Shinohara M, Toyokuni S, Morimoto T, Matsui S, Honjo T and Shinohara T: Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damage and serial transplantation. Biol Reprod. 68:1801–1807. 2003. View Article : Google Scholar : PubMed/NCBI
33	Siu ER, Mruk DD, Porto CS and Cheng CY: Cadmium-induced testicular injury. Toxicol Appl Pharmacol. 238:240–249. 2009. View Article : Google Scholar : PubMed/NCBI
34	Koksal IT, Ishak Y, Usta M, Danisman A, Guntekin E, Bassorgun IC and Ciftcioglu A: Varicocele-induced testicular dysfunction may be associated with disruption of blood-testis barrier. Arch Androl. 53:43–48. 2007. View Article : Google Scholar : PubMed/NCBI
35	Erkanlı Şentürk G, Ersoy Canillioglu Y, Umay C, Demiralp-Eksioglu E and Ercan F: Distribution of Zonula Occludens-1 and Occludin and alterations of testicular morphology after in utero radiation and postnatal hyperthermia in rats. Int J Exp Pathol. 93:438–449. 2012. View Article : Google Scholar
36	Xia W, Wong EW, Mruk DD and Cheng CY: TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins: A new concept of BTB regulation during spermatogenesis. Dev Biol. 327:48–61. 2009. View Article : Google Scholar :