Mice overexpression of human augmenter of liver regeneration (hALR) in male germ cells shows abnormal spermatogenesis and reduced fertility

Endocrine Journal

Volumn 59, Issue 11, 2012, Pages 989-999

  Cao, Yan ^a   Fu, Yu Long ^a   Ge, Chang Hui ^a,b   Xu, Wang Xiang ^a,b   Zhan, Yi Qun ^a,b   Li, Chang Yan ^a,b   Li, Wei ^a,b   Wang, Xiao Hui ^a,b   Wang, Zhi Dong ^a,b   Yu, Miao ^a,b   Yang, Xiao Ming ^a,b  

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^b State Key Laboratory of Proteomics   (China)

Author keywords

Apoptosis; Augmenter of liver regeneration; Male fertility; Spermatocytes

Indexed keywords

HEPATOPOIETIN; HUMAN AUGMENTER OF LIVER REGENERATION; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL POPULATION; CELL VACUOLE; GENE OVEREXPRESSION; GERM CELL; HAPLOIDY; HISTOPATHOLOGY; MALE; MALE FERTILITY; MALE INFERTILITY; MOUSE; NICK END LABELING; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; SPERMATOCYTE; SPERMATOGENESIS; TESTIS DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; CYTOCHROME REDUCTASES; HUMANS; INFERTILITY, MALE; MALE; MICE; MICE, TRANSGENIC; OLIGOSPERMIA; SPERMATOGENESIS; TESTIS;

EID: 84871067788     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.EJ12-0160     Document Type: Article

References (40)

1. Rajender S, Rahul P, Mahdi AA (2010) Mitochondria, spermatogenesis and male infertility. Mitochondrion 10: 419-428.
2. St John JC, Sakkas D, Barratt CL (2000) A role for mitochondrial DNA and sperm survival. J Androl 21: 189-199.
3. Rantanen A, Jansson M, Oldfors A, Larsson NG (2001) Downregulation of Tfam and mtDNA copy number during mammalian spermatogenesis. Mamm Genome 12: 787-792.
4. Xu G, Vogel KS, McMahan CA, Herbert DC, Walter CA (2010) BAX and tumor suppressor TRP53 are important in regulating mutagenesis in spermatogenic Cells in mice. Biol Reprod 83: 979-987.
5. Nakada K, Sato A, Yoshida K, Morita T, Tanaka H, et al. (2006) Mitochondria-related male infertility. Proc Natl Acad Sci U S A 103: 15148-15153.
6. Shamsi MB, Kumar R, Bhatt A, Bamezai RN, Gupta NP, et al. (2008) Mitochondrial DNA Mutations in etiopathogenesis of male infertility. Indian J Urol 24: 150-154.
7. Lisowsky T, Lee JE, Polimeno L, Francavilla A, Hofhaus G (2001) Mammalian augmenter of liver regeneration protein is a sulfhydryl oxidase. Dig Liver Dis 33: 173-180.
8. Coppock DL, Thorpe C (2006) Multidomain flavindependent sulfhydryl oxidases. Antioxid Redox Signal 8: 300-311.
9. Lill R, Muhlenhoff U (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu Rev Cell Dev Biol 22: 457-486.
10. Lange H, Lisowsky T, Gerber J, Muhlenhoff U, Kispal G, et al. (2001) An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2: 715-720.
11. Dayoub R, Wagner H, Bataille F, Stoltzing O, Spruss T, et al. (2011) Liver regeneration associated protein (ALR) exhibits antimetastatic potential in hepatocellular carcinoma. Mol Med 17: 221-228.
12. Hell K (2008) The Erv1-Mia40 disulfide relay system in the intermembrane space of mitochondria. Biochim Biophys Acta 1783: 601-609.
13. Lisowsky T (1994) ERV1 is involved in the cell-division cycle and the maintenance of mitochondrial genomes in Saccharomyces cerevisiae. Curr Genet 26: 15-20.
14. Polimeno L, Pesetti B, Lisowsky T, Iannone F, Resta L, et al. (2009) Protective effect of augmenter of liver regeneration on hydrogen peroxide-induced apoptosis in SH-SY5Y human neuroblastoma cells. Free Radic Res 43: 865-875.
15. Cao Y, Fu YL, Yu M, Yue PB, Ge CH, et al. (2009) Human augmenter of liver regeneration is important for hepatoma cell viability and resistance to radiation-induced oxidative stress. Free Radic Biol Med 47: 1057-1066.
16. Sankar U, Means AR (2011) Gfer is a critical regulator of HSC proliferation. Cell Cycle 10: 2263-2268.
17. Rouault TA, Tong WH (2005) Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6: 345-351.
18. Polimeno L, Capuano F, Marangi LC, Margiotta M, Lisowsky T, et al. (2000) The augmenter of liver regeneration induces mitochondrial gene expression in rat liver and enhances oxidative phosphorylation capacity of liver mitochondria. Dig Liver Dis 32: 510-517.
19. Polimeno L, Pesetti B, Giorgio F, Moretti B, Resta L, et al. (2009) Expression and localization of augmenter of liver regeneration in human muscle tissue. Int J Exp Pathol 90: 423-430.
20. Klissenbauer M, Winters S, Heinlein UA, Lisowsky T (2002) Accumulation of the mitochondrial form of the sulphydryl oxidase Erv1p/Alrp during the early stages of spermatogenesis. J Exp Biol 205: 1979-1986.
21. Kumari M, Aumuller G, Bergmann M, Meinhardt A, Seitz J (1990) Stage-dependent appearance of sulfhydryl oxidase during spermatogenesis in the testis of rat and hamster. An immunohistochemical study. Histochemistry 94: 365-371.
22. Tury A, Mairet-Coello G, Lisowsky T, Griffond B, Fellmann D (2005) Expression of the sulfhydryl oxidase ALR (Augmenter of Liver Regeneration) in adult rat brain. Brain Res 1048: 87-97.
23. Dayoub R, Groitl P, Dobner T, Bosserhoff AK, Schlitt HJ, et al. (2010) Foxa2 (HNF-3beta) regulates expression of hepatotrophic factor ALR in liver cells. Biochem Biophys Res Commun 395: 465-470.
24. Kobayashi T, Kaneko T, Iuchi Y, Matsuki S, Takahashi M, et al. (2002) Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in reproductive tracts and spermatozoa of male rats. J Androl 23: 674-683.
25. Chen X, Zhang DY, Liu X, Wei GH (2007) [Expression of augmenter of liver regeneration in cryptorchidism spermatogenic cells and its implication]. Zhonghua Nan Ke Xue 13: 700-705 (In Chinese).
26. Skawran B, Schubert S, Dechend F, Vervoorts J, Nayernia K, et al. (2005) Characterization of a human TSPY promoter. Mol Cell Biochem 276: 159-167.
27. Kido T, Lau YF (2005) A Cre gene directed by a human TSPY promoter is specific for germ cells and neurons. Genesis 42: 263-275.
28. Yu Z, Ji P, Cao J, Zhu S, Li Y, et al. (2009) Dazl promotes germ cell differentiation from embryonic stem cells. J Mol Cell Biol 1: 93-103.
29. Li B, Nair M, Mackay DR, Bilanchone V, Hu M, et al. (2005) Ovol1 regulates meiotic pachytene progressionduring spermatogenesis by repressing Id2 expression. Development 132: 1463-1473.
30. Di Agostino S, Botti F, Di Carlo A, Sette C, Geremia R (2004) Meiotic progression of isolated mouse spermatocytes under simulated microgravity. Reproduction 128: 25-32.
31. Howarth DG, Donoghue MJ (2009) Duplications and expression of DIVARICATA-like genes in dipsacales. Mol Biol Evol 26: 1245-1258.
32. van Montfoort AP, Geraedts JP, Dumoulin JC, Stassen AP, Evers JL, et al. (2008) Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. Mol Hum Reprod 14: 157-168.
33. Meinhardt A, Wilhelm B, Seitz J (1999) Expression of mitochondrial marker proteins during spermatogenesis. Hum Reprod Update 5: 108-119.
34. Perl A, Qian Y, Chohan KR, Shirley CR, Amidon W, et al. (2006) Transaldolase is essential for maintenance of the mitochondrial transmembrane potential and fertility of spermatozoa. Proc Natl Acad Sci U S A 103: 14813-14818.
35. Todd LR, Gomathinayagam R, Sankar U (2010) A novel Gfer-Drp1 link in preserving mitochondrial dynamics and function in pluripotent stem cells. Autophagy 6: 821-822.
36. Martincic DS, Virant Klun I, Zorn B, Vrtovec HM (2001) Germ cell apoptosis in the human testis. Pflugers Arch 442: R159-160.
37. Levy R, Seifer-Aknin I (2001) [Apoptosis during spermatogenesis and in ejaculated spermatozoa: importance for fertilization]. Ann Biol Clin (Paris) 59: 531-545 (In French).
38. Print CG, Loveland KL (2000) Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays 22: 423-430.
39. Nakai A, Suzuki M and Tanabe M (2000) Arrest of spermatogenesis in mice expressing an active heat shock transcription factor 1. EMBO J 19: 1545-1554.
40. Shiraishi K, Naito K, Yoshida K (2000) Inhibition of calpain but not caspase protects the testis against injury after experimental testicular torsion of rat. Biol Reprod 63: 1538-1548.