Comparative proteomic analysis of different developmental stages of swamp buffalo testicular seminiferous tubules

With ageing, many protein components change markedly during mammalian spermatogenesis. Most of these proteins have yet to be characterized and verified. Here, we have employed two-dimensional electrophoresis coupled to tandem mass spectrometry to explore the different proteins from pre-pubertal, pubertal and post-pubertal swamp buffalo testicular seminiferous tubules. The results showed that 25 protein spots were differentially expressed among developmental stages, and 13 of them were successfully identified by mass spectrometry. Of which four proteins were up-regulated and three proteins were down-regulated with age, and the remaining six proteins were fluctuated among developmental stages. Bioinformatics analysis indicates that these proteins were probably related to cellular developmental process (53.8%), cell differentiation (53.8%), spermatogenesis (15.4%), apoptotic process and cell death (30.8%). Expression profiles of calumenin (CALU) and galectin-1 (LGALS1) were further verified via Western blotting. In summary, the results help to develop an understanding of molecular mechanisms associated with buffalo spermatogenesis.

[1]  T. Mipam,et al.  Comparative testis proteome of cattleyak from different developmental stages. , 2017, Animal : an international journal of animal bioscience.

[2]  Ming Zhang,et al.  Spermatogenesis‐associated proteins at different developmental stages of buffalo testicular seminiferous tubules identified by comparative proteomic analysis , 2016, Proteomics.

[3]  Yulin Huang,et al.  Proteome Profile and Quantitative Proteomic Analysis of Buffalo (Bubalusbubalis) Follicular Fluid during Follicle Development , 2016, International journal of molecular sciences.

[4]  Ming Zhang,et al.  Comparative Proteomic Analysis of Mature and Immature Oocytes of the Swamp Buffalo (Bubalus bubalis) , 2016, International journal of molecular sciences.

[5]  Holly J. Butler,et al.  The title of the paper 4-Nonylphenol induces disruption of spermatogenesis associated with oxidative stress-related apoptosis by targeting p 53-Bcl-2 / Bax-Fas / FasL signalling The short title 4-nonylphenol induces reproductive toxicity in male rats The full names of the authors , 2016 .

[6]  Wan-Xi Yang,et al.  The potential function of prohibitin during spermatogenesis in Chinese fire-bellied newt Cynops orientalis , 2015, Cell and Tissue Research.

[7]  J. Teng,et al.  Calumenin and fibulin-1 on tumor metastasis: Implications for pharmacology. , 2015, Pharmacological research.

[8]  Q. Fu,et al.  Differences between high- and low-motility buffalo sperm identified by comparative proteomics. , 2015, Reproduction in domestic animals = Zuchthygiene.

[9]  Xuejiang Guo,et al.  Unraveling the proteomic profile of mice testis during the initiation of meiosis. , 2015, Journal of Proteomics.

[10]  M. J. Freitas,et al.  Phosphoprotein phosphatase 1 complexes in spermatogenesis. , 2015, Current molecular pharmacology.

[11]  M. Hesse,et al.  HSP70-binding protein HSPBP1 regulates chaperone expression at a posttranslational level and is essential for spermatogenesis , 2014, Molecular biology of the cell.

[12]  C. Pineau,et al.  Proteomics and integrative genomics for unraveling the mysteries of spermatogenesis: the strategies of a team. , 2014, Journal of proteomics.

[13]  Xuejiang Guo,et al.  Establishment of a proteomic profile associated with gonocyte and spermatogonial stem cell maturation and differentiation in neonatal mice , 2014, Proteomics.

[14]  T. Egli,et al.  Poly(4-hydroxybutyrate) (P4HB) production in recombinant Escherichia coli: P4HB synthesis is uncoupled with cell growth , 2013, Microbial Cell Factories.

[15]  Q. Wang,et al.  Calumenin-15 facilitates filopodia formation by promoting TGF-β superfamily cytokine GDF-15 transcription , 2013, Cell Death and Disease.

[16]  D. H. Kim,et al.  Calumenin has a role in the alleviation of ER stress in neonatal rat cardiomyocytes. , 2013, Biochemical and biophysical research communications.

[17]  Yang Wang,et al.  Characterization of Cherax quadricarinatus prohibitin and its potential role in spermatogenesis. , 2013, Gene.

[18]  K. Moley,et al.  Molecular Analysis of Cell Type-Specific Gene Expression Profile During Mouse Spermatogenesis by Laser Microdissection and qRT-PCR , 2013, Reproductive Sciences.

[19]  H. Orozco,et al.  Genetic manipulation of longevity-related genes as a tool to regulate yeast life span and metabolite production during winemaking , 2013, Microbial Cell Factories.

[20]  C. Pineau,et al.  Spermatogenesis in mammals: proteomic insights , 2012, Systems biology in reproductive medicine.

[21]  Wan-Xi Yang,et al.  Characterization and expression analysis of prohibitin in the testis of Chinese mitten crab Eriocheir sinensis , 2012, Molecular Biology Reports.

[22]  W. Sieghart,et al.  Spatio-temporal expression analysis of the calcium-binding protein calumenin in the rodent brain , 2012, Neuroscience.

[23]  Hsiao-Fang Sunny Sun,et al.  Differential expression of porcine testis proteins during postnatal development. , 2011, Animal reproduction science.

[24]  Daniel Faria,et al.  Serum proteomics signature of cystic fibrosis patients: a complementary 2-DE and LC-MS/MS approach. , 2011, Journal of proteomics.

[25]  E. Nieschlag,et al.  Physiology of Testicular Function , 2010 .

[26]  D. H. Kim,et al.  Characterization of Calumenin-SERCA2 Interaction in Mouse Cardiac Sarcoplasmic Reticulum* , 2009, The Journal of Biological Chemistry.

[27]  Nobuaki Takemori,et al.  Proteome mapping of the Drosophila melanogaster male reproductive system , 2009, Proteomics.

[28]  B. Honoré.  The rapidly expanding CREC protein family: members, localization, function, and role in disease , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[29]  Xuejiang Guo,et al.  Analysis of the human testis proteome by mass spectrometry and bioinformatics , 2008, Proteomics. Clinical applications.

[30]  Xuejiang Guo,et al.  Proteomic analysis of testis biopsies in men treated with injectable testosterone undecanoate alone or in combination with oral levonorgestrel as potential male contraceptive. , 2008, Journal of proteome research.

[31]  Xinru Wang,et al.  Construction of a proteome profile and functional analysis of the proteins involved in the initiation of mouse spermatogenesis. , 2008, Journal of proteome research.

[32]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[33]  J. Garin,et al.  Post-meiotic Shifts in HSPA2/HSP70.2 Chaperone Activity during Mouse Spermatogenesis* , 2006, Journal of Biological Chemistry.

[34]  M. Paz,et al.  Proteome profile changes during mouse testis development. , 2006, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[35]  R. Kiss,et al.  Galectin-1: a small protein with major functions. , 2006, Glycobiology.

[36]  Xuejiang Guo,et al.  Proteomic analysis of effect of hyperthermia on spermatogenesis in adult male mice. , 2006, Journal of proteome research.

[37]  C. Pineau,et al.  Identification, molecular cloning, and cellular distribution of the rat homolog of minichromosome maintenance protein 7 (MCM7) in the rat testis , 2006, Molecular reproduction and development.

[38]  P. Nachtigal,et al.  Vimentin expression during altered spermatogenesis in rats. , 2005, Acta histochemica.

[39]  San-Yuan Huang,et al.  A reference map and identification of porcine testis proteins using 2‐DE and MS , 2005, Proteomics.

[40]  Y. Ikeda,et al.  Accelerated impairment of spermatogenic cells in sod1-knockout mice under heat stress , 2005, Free radical research.

[41]  G. Rabinovich,et al.  Regulated Expression and Ultrastructural Localization of Galectin-1, a Proapoptotic β-Galactoside-Binding Lectin, During Spermatogenesis in Rat Testis1 , 2003, Biology of reproduction.

[42]  G. Rabinovich,et al.  Unlocking the secrets of galectins: a challenge at the frontier of glyco‐immunology , 2002, Journal of leukocyte biology.

[43]  C. Pineau,et al.  Proteome analysis of rat spermatogonia: Reinvestigation of stathmin spatio‐temporal expression within the testis , 2001, Molecular reproduction and development.

[44]  C. Pineau,et al.  Cellular distribution of translationally controlled tumor protein in rat and human testes , 2001, Proteomics.

[45]  R. Wait,et al.  A modified silver staining protocol for visualization of proteins compatible with matrix‐assisted laser desorption/ionization and electrospray ionization‐ mass spectrometry , 2000, Electrophoresis.

[46]  B. Honoré,et al.  The CREC family, a novel family of multiple EF‐hand, low‐affinity Ca2+‐binding proteins localised to the secretory pathway of mammalian cells , 2000, FEBS letters.

[47]  E. Robertson,et al.  Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. , 1993, Development.