Subunits of cyclic adenosine 3',5'-monophosphate-dependent protein kinase show differential and distinct expression patterns during germ cell differentiation: alternative polyadenylation in germ cells gives rise to unique smaller-sized mRNA species.

Cyclic AMP (cAMP) and cAMP-dependent protein kinases (PKAs) are believed to be involved in the regulation of essential spermatozoal functions, such as motility, epididymal maturation, capacitation, and the acrosome reaction. In this study, we document the presence of significant mRNA levels for 5 different PKA subunits (RI alpha, RI beta, RII alpha, RII beta, and C alpha) in germ cells and demonstrate differential expression patterns for these subunits during spermatogenesis. Messenger RNAs for RI (RI alpha and RI beta) and C alpha appear to be induced at premeiotic germ cell stages, whereas mRNAs for RII (RII alpha and RII beta) are first expressed at haploid stages. The individual PKA subunits may convey specific functions in developing germ cells and mature sperm. The present study, furthermore, demonstrates the presence of unique smaller-sized mRNAs in germ cells compared with somatic cells. Specific, truncated forms of RI alpha, RII alpha, RII beta, and C alpha mRNAs appear to be selected in the germ cells. Our data suggest this to be due to the use of alternative polyadenylation site signals. The selection of shorter mRNA species, with higher stability, may be essential for the delayed translation observed in spermatids. This may ensure certain levels of mRNA for translation at late spermatid stages, after cessation of transcription.

[1]  S. Beebe,et al.  Molecular cloning of a tissue-specific protein kinase (C gamma) from human testis--representing a third isoform for the catalytic subunit of cAMP-dependent protein kinase. , 1990, Molecular endocrinology.

[2]  A. Means,et al.  Analysis of expression of multiple genes encoding calmodulin during spermatogenesis. , 1989, Molecular endocrinology.

[3]  T. Jahnsen,et al.  Differential expression and subcellular localization for subunits of cAMP-dependent protein kinase during ram spermatogenesis , 1989, The Journal of cell biology.

[4]  John D. Scott,et al.  Human testis cDNA for the regulatory subunit RIIα of CAMP‐dependent protein kinase encodes an alternate amino‐terminal region , 1989, FEBS letters.

[5]  F. Levy,et al.  Molecular cloning, complementary deoxyribonucleic acid structure and predicted full-length amino acid sequence of the hormone-inducible regulatory subunit of 3'-5'-cyclic adenosine monophosphate-dependent protein kinase from human testis. , 1988, Molecular endocrinology.

[6]  S. Hanks,et al.  A cDNA clone encoding human cAMP-dependent protein kinase catalytic subunit C alpha. , 1988, Nucleic acids research.

[7]  R. Rickles,et al.  Antisense RNA directed against the 3' noncoding region prevents dormant mRNA activation in mouse oocytes. , 1988, Science.

[8]  M. Paupard,et al.  Major 56,000‐dalton, soluble phosphoprotein present in bovine sperm is the regulatory subunit of a type II cAMP‐dependent protein kinase , 1988, Journal of cellular biochemistry.

[9]  G. McKnight,et al.  Genetic characterization of a brain-specific form of the type I regulatory subunit of cAMP-dependent protein kinase. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[10]  E. Krebs,et al.  A unique mRNA species for a regulatory subunit of cAMP‐dependent protein kinase is specifically induced in haploid germ cells , 1988, FEBS letters.

[11]  W. Wasco,et al.  Interaction of the regulatory subunit of a type II cAMP-dependent protein kinase with mammalian sperm flagellum. , 1988, The Journal of biological chemistry.

[12]  T. Agthoven,et al.  Molecular characterization of the testis specific c‐abl mRNA in mouse. , 1987, The EMBO journal.

[13]  T. Jahnsen,et al.  Cellular localization and age-dependent changes in mRNA for cyclic adenosine 3',5'-monophosphate-dependent protein kinases in rat testis. , 1987, Biology of reproduction.

[14]  C. Brokaw A lithium-sensitive regulator of sperm flagellar oscillation is activated by cAMP-dependent phosphorylation , 1987, The Journal of cell biology.

[15]  W. Kistler,et al.  Transcriptional and translational control of the message for transition protein 1, a major chromosomal protein of mammalian spermatids. , 1987, The Journal of biological chemistry.

[16]  E. Krebs,et al.  The molecular cloning of a type II regulatory subunit of the cAMP-dependent protein kinase from rat skeletal muscle and mouse brain. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Brosius,et al.  Rat calmodulin cDNA. , 1987, DNA.

[18]  D. Nielsen,et al.  Regulation of messenger RNA stability in eukaryotic cells , 1987, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  R. Maurer,et al.  A cloned bovine cDNA encodes an alternate form of the catalytic subunit of cAMP-dependent protein kinase. , 1986, The Journal of biological chemistry.

[20]  M. Uhler,et al.  Evidence for a second isoform of the catalytic subunit of cAMP-dependent protein kinase. , 1986, The Journal of biological chemistry.

[21]  U. Walter,et al.  Molecular cloning, cDNA structure, and regulation of the regulatory subunit of type II cAMP-dependent protein kinase from rat ovarian granulosa cells. , 1986, The Journal of biological chemistry.

[22]  G. Shaw,et al.  A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation , 1986, Cell.

[23]  H. Hidaka,et al.  Axokinin phosphorylation by cAMP-dependent protein kinase is sufficient for activation of sperm flagellar motility , 1986, The Journal of cell biology.

[24]  P. De Camilli,et al.  Heterogeneous distribution of the cAMP receptor protein RII in the nervous system: evidence for its intracellular accumulation on microtubules, microtubule-organizing centers, and in the area of the Golgi complex , 1986, The Journal of cell biology.

[25]  E. Krebs,et al.  Isolation of cDNA clones coding for the catalytic subunit of mouse cAMP-dependent protein kinase. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Atherton,et al.  A study of rat epididymal sperm adenosine 3',5'-monophosphate-dependent protein kinases: maturation differences and cellular location. , 1985, Biology of reproduction.

[27]  U. Walter,et al.  High-affinity binding of the regulatory subunit (RII) of cAMP-dependent protein kinase to microtubule-associated and other cellular proteins. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[28]  N. Hecht,et al.  Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. , 1984, Developmental biology.

[29]  S. Berget Are U4 small nuclear ribonucleoproteins involved in polyadenylation? , 1984, Nature.

[30]  H. Toeg,et al.  Characterization and localization of cAMP-dependent protein kinases in rat caudal epididymal sperm. , 1984, The Journal of biological chemistry.

[31]  E. Krebs,et al.  Isolation of a cDNA clone for the type I regulatory subunit of bovine cAMP-dependent protein kinase. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Conti,et al.  Developmental changes of cyclic adenosine monophosphate-dependent protein kinase activity during spermatogenesis in the mouse. , 1983, Biology of reproduction.

[33]  A. Means,et al.  Cyclic adenosine 3',5' monophosphate, calcium and protein phosphorylation in flagellar motility. , 1983, Biology of reproduction.

[34]  Sinclair Gd,et al.  Purification and characterization of cytoplasmic protamine messenger ribonucleoprotein particles from rainbow trout testis cells. , 1982, Biochemistry.

[35]  G. Sinclair,et al.  Purification and characterization of cytoplasmic protamine messenger ribonucleoprotein particles from rainbow trout testis cells. , 1982, Biochemistry.

[36]  M. Dibartolomeis,et al.  A protein kinase bound to the projection portion of MAP 2 (microtubule-associated protein 2) , 1981, The Journal of cell biology.

[37]  Kopf Gs,et al.  The regulation of spermatozoa by calcium cyclic nucleotides. , 1980 .

[38]  D. Garbers,et al.  The regulation of spermatozoa by calcium cyclic nucleotides. , 1980, Advances in cyclic nucleotide research.

[39]  Russell Dh Type I cyclic AMP-dependent protein kinase as a positive effector of growth. , 1978 .

[40]  J. Grootegoed,et al.  Ribonucleic acid synthesis in vitro in primary spermatocytes isolated from rat testis. , 1977, The Biochemical journal.

[41]  M. Conti,et al.  RNA synthesis in spermatocytes and spermatids and preservation of meiotic RNA during spermiogenesis in the mouse. , 1977, Cell differentiation.

[42]  W. Gilbert,et al.  A new method for sequencing DNA. , 1977, Proceedings of the National Academy of Sciences of the United States of America.