Three testis-specific paralogous serine proteases play different roles in murine spermatogenesis and are involved in germ cell survival during meiosis

Biology of Reproduction

Volumn 88, Issue 5, 2013, Pages

  Yoneda, Ryoma ^a   Takahashi, Takayuki ^a   Matsui, Hitoshi ^a   Takano, Naoharu ^a   Hasebe, Yuko ^a   Ogiwara, Katsueki ^a   Kimura, Atsushi P ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Apoptosis; Germ cell; Localization; Meiosis; Organ culture; Protease; Prss; Spermatogenesis; Tessp

Indexed keywords

SERINE PROTEINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; GENE CLUSTER; MALE; MEIOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS;

APOPTOSIS; GERM CELL; LOCALIZATION; MEIOSIS; ORGAN CULTURE; PROTEASE; PRSS; SPERMATOGENESIS; TESSP;

ANIMALS; APOPTOSIS; CELL SURVIVAL; MALE; MEIOSIS; MICE; ORGAN CULTURE TECHNIQUES; SERINE PROTEASES; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 84880974399     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.106328     Document Type: Article

References (70)

1. Yoshida S. Spermatogenic stem cell system in the mouse testis. Cold Spring Harb Symp Quant Biol 2008; 73:25-32.
2. Steger K, Klonisch T, Gavenis K, Behr R, Schaller V, Drabent B, Doenecke D, Nieschlag E, Bergmann M, Weinbauer GF. Round spermatids show normal testis-specific H1t but reduced cAMP-responsive element modulator and transition protein 1 expression in men with roundspermatid maturation arrest. J Androl 1999; 20:747-754.
3. Cheng CY, Mruk DD. Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem J 2011; 435:553-562.
4. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 2000; 163:3-9.
5. De Felici M, Farini D, Dolci S. In or out stemness: comparing growth factor signalling in mouse embryonic stem cells and primordial germ cells. Curr Stem Cell Res Ther 2009; 4:87-97.
6. Wakayama T, Iseki S. Role of the spermatogenic-Sertoli cell interaction through cell adhesion molecule-1 (CADM1) in spermatogenesis. Anat Sci Int 2009; 84:112-121.
7. Kopera IA, Bilinska B, Cheng CY, Mruk DD. Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 2010; 365:1593-1605.
8. Goldberg RB, Geremia R, Bruce WR. Histone synthesis and replacement during spermatogenesis in the mouse. Differentiation 1977; 7:167-180.
9. Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 2010; 139:287-301.
10. Gaucher J, Reynoird N, Montellier E, Boussouar F, Rousseaux S, Khochbin S. From meiosis to postmeiotic events: the secrets of histone disappearance. FEBS J 2010; 277:599-604.
11. Odet F, Verot A, Le Magueresse-Battistoni B. The mouse testis is the source of various serine proteases and serine proteinase inhibitors (SERPINs): Serine proteases and SERPINs identified in Leydig cells are under gonadotropin regulation. Endocrinology 2006; 147:4374-4383.
12. Le Magueresse-Battistoni B. Serine proteases and serine protease inhibitors in testicular physiology: the plasminogen activation system. Reproduction 2007; 134:721-729.
13. Netzel-Arnett S, Bugge TH, Hess RA, Carnes K, Stringer BW, Scarman AL, Hooper JD, Tonks ID, Kay GF, Antalis TM. The glycosylphosphatidylinositol- anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability. Biol Reprod 2009; 81:921-932.
14. Liu YX. Involvement of plasminogen activator and plasminogen activator inhibitor type 1 in spermatogenesis, sperm capacitation, and fertilization. Semin Thromb Hemost 2007; 33:29-40.
15. Lacroix M, Smith FE, Fritz IB. Changes in levels of plasminogen activator activity in normal and germ-cell-depleted testes during development. Mol Cell Endocrinol 1982; 26:259-267.
16. Honda A, Siruntawineti J, Baba T. Role of acrosomal matrix proteases in sperm-zona pellucida interactions. Hum Reprod Update 2002; 8:405-412.
17. Buffone MG, Foster JA, Gerton GL. The role of the acrosomal matrix in fertilization. Int J Dev Biol 2008; 52:511-522.
18. Han C, Kwon JT, Park I, Lee B, Jin S, Choi H, Cho C. Impaired sperm aggregation in Adam2 and Adam3 null mice. Fertil Steril 2010; 93: 2754-2756.
19. Igdoura SA, Morales CR, Hermo L. Differential expression of cathepsins B and D in testis and epididymis of adult rats. J Histochem Cytochem 1995; 43:545-557.
20. Kimura A, Matsui H, Takahashi T. Expression and localization of prolyl oligopeptidase in mouse testis and its possible involvement in sperm motility. Zoolog Sci 2002; 19:93-102.
21. Ou CM, Lin SR, Lin HJ, Luo CW, Chen YH. Exclusive expression of a membrane-bound Spink3-interacting serine protease-like protein TESPL in mouse testis. J Cell Biochem 2010; 110:620-629.
22. Uhrin P, Dewerchin M, Hilpert M, Chrenek P, Schofer C, Zechmeister- Machhart M, Kronke G, Vales A, Carmeliet P, Binder BR, Geiger M. Disruption of the protein C inhibitor gene results in impaired spermatogenesis and male infertility. J Clin Invest 2000; 106:1531-1539.
23. Lee B, Park I, Jin S, Choi H, Kwon JT, Kim J, Jeong J, Cho BN, Eddy EM, Cho C. Impaired spermatogenesis and fertility in mice carrying a mutation in the Spink2 gene expressed predominantly in testes. J Biol Chem 2011; 286:29108-29117.
24. Takano N, Matusi H, Takahashi T. Granzyme N, a novel granzyme, is expressed in spermatocytes and spermatids of the mouse testis. Biol Reprod 2004; 71:1785-1795.
25. Xu HP, Yuan L, Shan J, Feng H. Localization and expression of TSP50 protein in human and rodent testes. Urology 2004; 64:826-832.
26. Ben-Aharon I, Brown PR, Etkovitz N, Eddy EM, Shalgi R. The expression of calpain 1 and calpain 2 in spermatogenic cells and spermatozoa of the mouse. Reproduction 2005; 129:435-442.
27. Ben-Aharon I, Brown PR, Shalgi R, Eddy EM. Calpain 11 is unique to mouse spermatogenic cells. Mol Reprod Dev 2006; 73:767-773.
28. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 2003; 4: 544-558.
29. Takano N, Matsui H, Takahashi T. TESSP-1: a novel serine protease gene expressed in the spermatogonia and spermatocytes of adult mouse testes. Mol Reprod Dev 2005; 70:1-10.
30. Takano N, Kimura A, Takahashi T. Two distinct localization patterns of testis-specific serine protease 1 (TESSP1) in the seminiferous tubules of the mouse testis. Zoolog Sci 2009; 26:294-300.
31. Wong GW, Yasuda S, Morokawa N, Li L, Stevens RL. Mouse chromosome 17A3.3 contains 13 genes that encode functional trypticlike serine proteases with distinct tissue and cell expression patterns. J Biol Chem 2004; 279:2438-2452.
32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28:2731-2739.
33. Matsubara S, Takahashi T, Kimura AP. Epigenetic patterns at the mouse prolyl oligopeptidase gene locus suggest the CpG island in the gene body to be a novel regulator for gene expression. Gene 2010; 465:17-29.
34. Matsubara S, Takahashi T, Kimura AP. Localization and subcellular distribution of prolyl oligopeptidase in the mouse placenta. J Mol Histol 2011; 42:251-264.
35. Bastos H, Lassalle B, Chicheportiche A, Riou L, Testart J, Allemand I, Fouchet P. Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 2005; 65:40-49.
36. Wu Y, Dowbenko D, Pisabarro MT, Dillard-Telm L, Koeppen H, Lasky LA. PTEN 2, a Golgi-associated testis-specific homologue of the PTEN tumor suppressor lipid phosphatase. J Biol Chem 2001; 276: 21745-21753.
37. Wang PJ, Page DC, McCarrey JR. Differential expression of sex-linked and autosomal germ-cell-specific genes during spermatogenesis in the mouse. Hum Mol Genet 2005; 14:2911-2918.
38. Abe K, Jin Y, Yamamoto T, Abe S. Human recombinant stem cell factor promotes spermatogonial proliferation, but not meiosis initiation in organ culture of newt testis fragments. Biochem Biophys Res Commun 2002; 294:695-699.
39. Zhang J, Eto K, Honmyou A, Nakao K, Kiyonari H, Abe S. Neuregulins are essential for spermatogonial proliferation and meiotic initiation in neonatal mouse testis. Development 2011; 138:3159-3168.
40. Goetz P, Chandley AC, Speed RM. Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse. J. Cell Sci 1984; 65:249-263.
41. Antalis TM, Buzza MS, Hodge KM, Hooper JD, Netzel-Arnett S. The cutting edge: membrane-anchored serine protease activities in the pericellular microenvironment. Biochem J 2010; 428:325-346.
42. Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T. Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci U S A 2005; 102:8442-8447.
43. Nishimura H, Myles DG, Primakoff P. Identification of an ADAM2- ADAM3 complex on the surface of mouse testicular germ cells and cauda epididymal sperm. J Biol Chem 2007; 282:17900-17907.
44. Gyamera-Acheampong C, Tantibhedhyangkul J, Weerachatyanukul W, Tadros H, Xu H, van de Loo JW, Pelletier RM, Tanphaichitr N, Mbikay M. Sperm from mice genetically deficient for the PCSK4 proteinase exhibit accelerated capacitation, precocious acrosome reaction, reducedbinding to egg zona pellucida, and impaired fertilizing ability. Biol Reprod 2006; 74:666-673.
45. Kawano N, Kang W, Yamashita M, Koga Y, Yamazaki T, Hata T, Miyado K, Baba T. Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro. Biol Reprod 2010; 83:359-369.
46. Zhu GZ, Gupta S, Myles DG, Primakoff P. Testase 1 (ADAM 24) a sperm surface metalloprotease is required for normal fertility in mice. Mol Reprod Dev 2009; 76:1106-1114.
47. Schafer M, Nayernia K, Engel W, Schafer U. Translational control in spermatogenesis. Dev Biol 1995; 172:344-352.
48. Yan W, Si Y, Slaymaker S, Li J, Zheng H, Young DL, Aslanian A, Saunders L, Verdin E, Charo IF. Zmynd15 encodes a histone deacetylasedependent transcriptional repressor essential for spermiogenesis and male fertility. J Biol Chem 2010; 285:31418-31426.
49. Morales CR, Kwon YK, Hecht NB. Cytoplasmic localization during storage and translation of the mRNAs of transition protein 1 and protamine 1, two translationally regulated transcripts of the mammalian testis. J Cell Sci 1991; 100(Pt 1):119-131.
50. Langford KG, Zhou Y, Russell LD, Wilcox JN, Bernstein KE. Regulated expression of testis angiotensin-converting enzyme during spermatogenesis in mice. Biol Reprod 1993; 48:1210-1218.
51. Honda A, Yamagata K, Sugiura S, Watanabe K, Baba T. A mouse serine protease TESP5 is selectively included into lipid rafts of sperm membrane presumably as a glycosylphosphatidylinositol-anchored protein. J Biol Chem 2002; 277:16976-16984.
52. Watanabe H, Kondoh G. Mouse sperm undergo GPI-anchored protein release associated with lipid raft reorganization and acrosome reaction to acquire fertility. J Cell Sci 2011; 124:2573-2581.
53. Koyama K, Hasegawa A, Komori S. Functional aspects of CD52 in reproduction. J Reprod Immunol 2009; 83:56-59.
54. Maruyama M, Yoshitake H, Tsukamoto H, Takamori K, Araki Y. Molecular expression of Ly6k, a putative glycosylphosphatidyl-inositolanchored membrane protein on the mouse testicular germ cells. Biochem Biophys Res Commun 2010; 402:75-81.
55. Pierleoni A, Martelli PL, Casadio R. PredGPI: a GPI-anchor predictor. BMC Bioinformatics 2008; 9:392.
56. Hunter D, Anand-Ivell R, Danner S, Ivell R. Models of in vitro spermatogenesis. Spermatogenesis 2012; 2:32-43.
57. Abu Elhija M, Lunenfeld E, Schlatt S, Huleihel M. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl 2012; 14:285-293.
58. van der Wee KS, Johnson EW, Dirami G, Dym TM, Hofmann MC. Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J Androl 2001; 22:696-704.
59. Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T. In vitro production of functional sperm in cultured neonatal mouse testes. Nature 2011; 471:504-507.
60. Nakai A, Suzuki M, Tanabe M. Arrest of spermatogenesis in mice expressing an active heat shock transcription factor 1. EMBO J 2000; 19: 1545-1554.
61. Date S, Nozawa O, Inoue H, Hidema S, Nishimori K. Impairment of pachytene spermatogenesis in dmrt7 deficient mice, possibly causing meiotic arrest. Biosci Biotechnol Biochem 2012; 76:1621-1626.
62. Russell LD, Ettlin RA, Sinha-Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. St. Louis, MO: Cache River Press; 1990:119-161.
63. Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the beta1 integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945-964.
64. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747-806.
65. Siu MK, Cheng CY. Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 2004; 26:978-992.
66. Pellegrini M, Grimaldi P, Rossi P, Geremia R, Dolci S. Developmental expression of BMP4/ALK3/SMAD5 signaling pathway in the mouse testis: a potential role of BMP4 in spermatogonia differentiation. J Cell Sci 2003; 116:3363-3372.
67. Zhao GQ, Liaw L, Hogan BL. Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 1998; 125:1103-1112.
68. Miura C, Ohta T, Ozaki Y, Tanaka H, Miura T. Trypsin is a multifunctional factor in spermatogenesis. Proc Natl Acad Sci U S A 2009; 106:20972-20977.
69. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002; 3:932-943.
70. Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W. Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 2007; 17:413-421.