Genes and proteins expressed specifically in testis


Principal Investigator :  Anil K Suri

Project Associates/Assistants
Nirmala Jagadish
R Selvi
Pragyan Roy

Collaborators
John C Herr, Univ Virginia, USA
K Koyama,
Hyogo College of Med, Japan

The goal of this project is to investigate testis specific genes expressed in a restricted, temporal and spatial manner during spermatogenesis. Morphological and biochemical observations along the molecular biological approaches suggest that germ cell differentiation is accompanied by selective gene expression. However, the molecular mechanisms regulating the cell type specifically gene expression during spermatogenesis are yet to be determined. Identification of testis specific genes and their characterization would thus enhance our understanding about the functioning of sperm at the molecular level. This would possibly highlight the mechanism of sperm development, sperm functioning, and sperm-egg interaction.

Characterization of A-kinase (PKRA) anchoring protein 4 (earlier called hi; AKAP 4, EMBL nomenclature) gene product:

Mammalian sperm motility is regulated by a cascade of cAMP-dependent protein phosphorylation events mediated by protein kinase A. A-kinase anchor proteins direct protein kinase A activity by tethering the enzyme near its physiologic substrates. The A-kinase anchor proteins (AKAPs) are a group of structurally diverse proteins, which have the common function of binding to the regulatory subunit of protein kinase A (PKA) and confining the holoenzyme to discrete locations within the cell. AKAP may be involved in the regulation of sperm motility.

In the course of identifying sperm proteins, we cloned the human hi mRNA from a testis cDNA expression library. This is referred as AKAP4 [A-kinase (PKRA) anchoring protein 4, EMBL nomenclature]. Peptides corresponding to target domain and regulatory domains were synthesized for motility studies. These peptides were conjugated with stearic acid. Inhibition of sperm motility was studied using various concentrations of peptides.

Characterization of SPAG9 (Sperm associated sperm antigen 9)

Characterization of the recombinant SPAG9: The recombinant SPAG9 expressed in E.coli revealed a major band at ~170 kDa in coomassie blue staining. Since the deduced molecular weight of SPAG9 is 83.9 kDa, the ~170 kDa molecular mass is apparently due to dimerization of protein. The antibodies to recombinant SPAG9 specifically recognized the recombinant protein in the western blot procedure, showing a single band of ~170 kDa. Proper folding and secondary structure of SPAG9 protein was investigated by the CD spectrum analysis. The CD spectra exhibited minima at 220 and 208, which is characteristic of a a-helical confirmation. The helical content calculated from CD spectra was found to be 40.2%, which was in agreement with the theoretical predictions of 41.38%.

Homologues of human SPAG9 gene: Homologue genes of SPAG9 were characterized from macaque and baboon. These results will have implications for understanding the basic biology of SPAG9. Macaque SPAG9 comprises of 2379 bp and has 94% and 92.2% homology with entire nucleotide sequence of hSPAG9 and baboon SPAG9, respectively. However, ORFs of macaque SPAG9 and human SPAG9 shared 95.5% identity. The macaque SPAG9 has inframe deletion of 93 bp starting at 1117 bp and 51 bp inframe deletion starting at 1770 bp as compared to human SPAG9. The macaque SPAG9 5’ UTR contains 110 nt having 100% identity with hSPAG9 whereas the macaque SPAG9 3’ UTR contains 130 nt as compared to 112 nt in hSAPG9. Sequence comparison of macaque 3’UTR, revealed 18 nucleotides deletion in 3’UTR of the hSPAG9. However, rest of the 3’UTR of macaque showed 100% identity. Significantly, the 5’ UTR and 3’ UTR in macaque SPAG9 has been conserved in the hSPAG9.

The amino acid sequence comparison of macaque SPAG9 with baboon and human SPAG9 revealed an overall homology of 87.0% (712/760 aa) and 84.9% (712/766 aa), respectively. However, when macaque N-terminal amino acid sequence (1-610 aa) was compared with baboon and human sequence, 100% identity with conserved functional domains namely JNK binding domain, leucine zipper motif, two coiled coil domains and a transmembrane domain was observed. It is noteworthy that macaque SPAG9 was found to have 31 amino acid deletions starting at 336 and another 17 amino acid deletion at 553 as compared to baboon and human. The carboxyl region of macaque SPAG9 expanding from 641 to 712 aa exhibited the great degree of difference and species conservation in comparison to baboon and human amino acids. Using genestream, align program, carboxyl region from 641 to 712 aa of macaque with 693 to 760 aa of baboon and 689 to 766 aa of human revealed a 29.6% (71/71aa) and 18.5% (71/77 aa) homology respectively.

Domain structure of SPAG9: The amino acid sequence analysis of SPAG9 showed the presence of a putative JNK binding domain (JBD), a characteristic leucine zipper motif (LZ), an extended coiled-coil domain (coil) and a transmembrane domain/lipoprotein binding domain site (T). GenBank database search indicated two entries describing structural homology to SPAG9. One cDNA encodes a predicted protein that has structural similarity to the C-terminal region and represent a fragment of JNK interacting protein 3 (JIP3). A second partial human cDNA also encodes a protein with similarity to C-terminus of SPAG9 but this protein is the product of distinct gene and may be related member of JIP3 group.

SPAG9 interaction with mammalian MAPKs: Structural homology analysis with JIP protein showed presence of signature domains of JNK interacting protein 3. Therefore, it was of interest to determine whether SPAG9 could also interact with MAPKs in a similar manner. The binding specificity of SPAG9 with various MAPKs was attempted in cotransfection experiments. Initial studies revealed that SPAG9 interacts with JNK1. Interaction of SPAG9 with JNK 2, JNK 3, ERK 2 or p38a in CHO cells is being carried out.

Role of SPAG9-JIP3g in human sperm-oocyte interaction: The involvement of SPAG9 protein in fertilization process was further confirmed by inhibition of sperm-zona interaction by its antibodies. Antibodies raised against the purified recombinant protein, that specifically recognized the recombinant as well as cognate SPAG9 protein on the Western blot, completely blocked sperm binding to zona pellucida of the human oocyte. Besides sperm zona interaction, it also seems to be involved in acrosome reaction of sperm that is prerequisite for fertilization. Inhibition of sperm attachment and tight binding with intact oocyte was observed in sperm treated with SPAG9 antibodies, whereas sperm incubated with preimmune serum did not inhibit the sperm attachment with zona pellucida. In hemi-zona assays, sperm treated with SPAG9-JIP3g antibody also revealed reduction in sperm attachment and tight binding as compared to sperm treated with preimmune serum. Therefore, SPAG9 sperm protein, in addition to mediating adherence and fusion, may also be involved in transducing signals into the oocyte at the time of gamete fusion which needs to be addressed in future studies.

SPAG9 protein and gene expression in panel of infertile men: Panel of infertile male semen samples was further screened for the presence of SPAG9 protein on sperm. The study revealed that in 75-semen sample, SPAG9 protein was localized but intensity of localization varied among the semen samples. However, it was also noted that 46 of the sperm sample did not show reactivity of SPAG9 indicating the absence of SPAG9 protein. Genomic analysis will be carried out in the subjects, which did not have SPAG9 protein. This may eventually explain the infertility related with SPAG9. The semen sample from fertile donor tested (112 samples) so far demonstrated the presence of SPAG9 protein.

SPAG9 gene function: Screening of mouse genomic library was carried out using SPAG9 cDNA probe. The 29 Kb mouse genomic clone was isolated successfully. Constructs were prepared deleting the exons coding for leucine zipper motif. Attempts will also be made to utilize short hairpin RNA interference (shRNAi) to rapidly determine if SPAG9 molecule is necessary for either sperm structure or sperm-egg interaction.

Publications

Original peer-reviewed articles

1.     Shankar S, Mohapatra B, Verma S, Selvi R, Jagadish N and Suri A (2004) Isolation and characterization of a haploid germ cell specific sperm associated antigen 9 (SPAG9) from the baboon. Mol Reprod Dev (in press).

Reviews/Proceedings

1.    Suri A (2004) Sperm specific proteins-potential candidate molecules for fertility control. Reprod Biol Endocrinol (in press).