{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T16:59:04Z","timestamp":1773853144934,"version":"3.50.1"},"reference-count":27,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2000,8,1]],"date-time":"2000-08-01T00:00:00Z","timestamp":965088000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nat Genet"],"published-print":{"date-parts":[[2000,8]]},"DOI":"10.1038\/78153","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T08:50:09Z","timestamp":1027673409000},"page":"448-452","source":"Crossref","is-referenced-by-count":193,"title":["Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4"],"prefix":"10.1038","volume":"25","author":[{"given":"Joy Y.","family":"Wu","sequence":"first","affiliation":[]},{"given":"Thomas J.","family":"Ribar","sequence":"additional","affiliation":[]},{"given":"David E.","family":"Cummings","sequence":"additional","affiliation":[]},{"given":"Kimberly A.","family":"Burton","sequence":"additional","affiliation":[]},{"given":"G. Stanley","family":"McKnight","sequence":"additional","affiliation":[]},{"given":"Anthony R.","family":"Means","sequence":"additional","affiliation":[]}],"member":"297","reference":[{"key":"BFng0800_448_CR1","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1126\/science.280.5367.1258","volume":"280","author":"RS Westphal","year":"1998","unstructured":"Westphal, R.S., Anderson, K.A., Means, A.R. & Wadzinski, B.E. A signaling complex of Ca2+-calmodulin-dependent protein kinase IV and protein phosphatase 2A. Science 280, 1258\u20131261 (1998).","journal-title":"Science"},{"key":"BFng0800_448_CR2","doi-asserted-by":"crossref","first-page":"15520","DOI":"10.1016\/S0021-9258(17)40710-1","volume":"269","author":"H Enslen","year":"1994","unstructured":"Enslen, H. et al. Characterization of Ca2+\/calmodulin-dependent protein kinase IV. Role in transcriptional regulation. J. Biol. Chem. 269, 15520\u201315527 (1994).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR3","doi-asserted-by":"publisher","first-page":"21542","DOI":"10.1074\/jbc.271.35.21542","volume":"271","author":"T Chatila","year":"1996","unstructured":"Chatila, T., Anderson, K.A., Ho, N. & Means, A.R. A unique phosphorylation-dependent mechanism for the activation of Ca2+\/calmodulin-dependent protein kinase type IV\/GR. J. Biol. Chem. 271, 21542\u201321548 (1996).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR4","doi-asserted-by":"publisher","first-page":"2527","DOI":"10.1101\/gad.8.21.2527","volume":"8","author":"P Sun","year":"1994","unstructured":"Sun, P., Enslen, H., Myung, P.S. & Maurer, R.A. Differential activation of CREB by Ca2+\/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8, 2527\u20132539 (1994).","journal-title":"Genes Dev."},{"key":"BFng0800_448_CR5","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1210\/mend.11.6.0011","volume":"11","author":"KA Anderson","year":"1997","unstructured":"Anderson, K.A., Ribar, T.J., Illario, M. & Means, A.R. Defective survival and activation of thymocytes in transgenic mice expressing a catalytically inactive form of Ca2+\/calmodulin-dependent protein kinase IV. Mol. Endocrinol. 11, 725\u2013737 (1997).","journal-title":"Mol. Endocrinol."},{"key":"BFng0800_448_CR6","doi-asserted-by":"publisher","first-page":"1203","DOI":"10.1016\/S0092-8674(00)81816-4","volume":"87","author":"H Bito","year":"1996","unstructured":"Bito, H., Deisseroth, K. & Tsien, R.W. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203\u20131214 (1996).","journal-title":"Cell"},{"key":"BFng0800_448_CR7","doi-asserted-by":"publisher","first-page":"7994","DOI":"10.1074\/jbc.275.11.7994","volume":"275","author":"JY Wu","year":"2000","unstructured":"Wu, J.Y. & Means, A.R. Ca2+\/calmodulin-dependent protein kinase IV is expressed in spermatids and targeted to chromatin and the nuclear matrix. J. Biol. Chem. 275, 7994\u20137999 (2000).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR8","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/0303-7207(76)90082-4","volume":"5","author":"KO Soderstrom","year":"1976","unstructured":"Soderstrom, K.O. & Parvinen, M. RNA synthesis in different stages of rat seminiferous epithelial cycle. Mol. Cell. Endocrinol. 5, 181\u2013199 (1976).","journal-title":"Mol. Cell. Endocrinol."},{"key":"BFng0800_448_CR9","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1128\/MCB.15.1.561","volume":"15","author":"Z Sun","year":"1995","unstructured":"Sun, Z., Sassone-Corsi, P. & Means, A.R. Calspermin gene transcription is regulated by two cyclic AMP response elements contained in an alternative promoter in the calmodulin kinase IV gene. Mol. Cell. Biol. 15, 561\u2013571 (1995).","journal-title":"Mol. Cell. Biol."},{"key":"BFng0800_448_CR10","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1038\/380162a0","volume":"380","author":"JA Blendy","year":"1996","unstructured":"Blendy, J.A., Kaestner, K.H., Weinbauer, G.F., Nieschlag, E. & Schutz, G. Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380, 162\u2013165 (1996).","journal-title":"Nature"},{"key":"BFng0800_448_CR11","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1038\/380159a0","volume":"380","author":"F Nantel","year":"1996","unstructured":"Nantel, F. et al. Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380, 159\u2013162 (1996).","journal-title":"Nature"},{"key":"BFng0800_448_CR12","first-page":"119","volume-title":"Histological and Histopathological Evaluation of the Testis","author":"LD Russell","year":"1990","unstructured":"Russell, L.D., Ettlin, R.A., Sinha Hikim, A.P. & Clegg, E.D. Histological and Histopathological Evaluation of the Testis 119\u2013161 (Cache River Press, Clearwater, Florida, 1990)."},{"key":"BFng0800_448_CR13","first-page":"165","volume-title":"Histones and Other Basic Nuclear Proteins","author":"ML Meistrich","year":"1989","unstructured":"Meistrich, M.L. Histone and basic nuclear protein transitions in mammalian spermatogenesis. in Histones and Other Basic Nuclear Proteins (eds Hnilica, L.S., Stein, G.S. & Stein, J.L.) 165\u2013182 (CRC Press, Boca Raton, Florida, 1989)."},{"key":"BFng0800_448_CR14","doi-asserted-by":"publisher","first-page":"12451","DOI":"10.1073\/pnas.92.26.12451","volume":"92","author":"K Lee","year":"1995","unstructured":"Lee, K., Haugen, H.S., Clegg, C.H. & Braun, R.E. Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. Proc. Natl Acad. Sci. USA 92, 12451\u201312455 (1995).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFng0800_448_CR15","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1038\/9684","volume":"22","author":"J Zhong","year":"1999","unstructured":"Zhong, J., Peters, A.H., Lee, K. & Braun, R.E. A double-stranded RNA binding protein required for activation of repressed messages in mammalian germ cells. Nature Genet. 22, 171\u2013174 (1999).","journal-title":"Nature Genet."},{"key":"BFng0800_448_CR16","doi-asserted-by":"publisher","first-page":"2173","DOI":"10.1128\/MCB.7.6.2173","volume":"7","author":"PC Yelick","year":"1987","unstructured":"Yelick, P.C. et al. Mouse protamine 2 is synthesized as a precursor whereas mouse protamine 1 is not. Mol. Cell. Biol. 7, 2173\u20132179 (1987).","journal-title":"Mol. Cell. Biol."},{"key":"BFng0800_448_CR17","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1002\/mrd.1080370303","volume":"37","author":"GR Green","year":"1994","unstructured":"Green, G.R., Balhorn, R., Poccia, D.L. & Hecht, N.B. Synthesis and processing of mammalian protamines and transition proteins. Mol. Reprod. Dev. 37, 255\u2013263 (1994).","journal-title":"Mol. Reprod. Dev."},{"key":"BFng0800_448_CR18","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1111\/j.1432-1033.1994.tb18979.x","volume":"223","author":"A Pirhonen","year":"1994","unstructured":"Pirhonen, A., Linnala-Kankkunen, A. & Menpaa, P.H. P2 protamines are phosphorylated in vitro by protein kinase C, whereas P1 protamines prefer cAMP-dependent protein kinase. A comparative study of five mammalian species. Eur. J. Biochem. 223, 165\u2013169 (1994).","journal-title":"Eur. J. Biochem."},{"key":"BFng0800_448_CR19","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1111\/j.1432-1033.1991.tb15800.x","volume":"196","author":"SM Elsevier","year":"1991","unstructured":"Elsevier, S.M., Noiran, J. & Carre-Eusebe, D. Processing of the precursor of protamine P2 in mouse. Identification of intermediates by their insolubility in the presence of sodium dodecyl sulfate. Eur. J. Biochem. 196, 167\u2013175 (1991).","journal-title":"Eur. J. Biochem."},{"key":"BFng0800_448_CR20","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1038\/12729","volume":"23","author":"X Xu","year":"1999","unstructured":"Xu, X., Toselli, P.A., Russell, L.D. & Seldin, D.C. Globozoospermia in mice lacking the casein kinase II a\u2032 catalytic subunit. Nature Genet. 23, 118\u2013121 (1999).","journal-title":"Nature Genet."},{"key":"BFng0800_448_CR21","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1002\/(SICI)1098-2795(199807)50:3<345::AID-MRD11>3.0.CO;2-3","volume":"50","author":"G Bench","year":"1998","unstructured":"Bench, G., Corzett, M.H., De Yebra, L., Oliva, R. & Balhorn, R. Protein and DNA contents in sperm from an infertile human male possessing protamine defects that vary over time. Mol. Reprod. Dev. 50, 345\u2013353 (1998).","journal-title":"Mol. Reprod. Dev."},{"key":"BFng0800_448_CR22","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/S0015-0282(98)00012-0","volume":"69","author":"L de Yebra","year":"1998","unstructured":"de Yebra, L. et al. Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil. Steril. 69, 755\u2013759 (1998).","journal-title":"Fertil. Steril."},{"key":"BFng0800_448_CR23","doi-asserted-by":"crossref","first-page":"9254","DOI":"10.1016\/S0021-9258(19)52538-8","volume":"256","author":"BP Kennedy","year":"1981","unstructured":"Kennedy, B.P. & Davies, P.L. Phosphorylation of a group of high molecular weight basic nuclear proteins during spermatogenesis in the winter flounder. J. Biol. Chem. 256, 9254\u20139259 (1981).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR24","doi-asserted-by":"crossref","first-page":"7962","DOI":"10.1016\/S0021-9258(20)81796-7","volume":"247","author":"AJ Louie","year":"1972","unstructured":"Louie, A.J. & Dixon, G.H. Kinetics of enzymatic modification of the protamines and a proposal for their binding to chromatin. J. Biol. Chem. 247, 7962\u20137968 (1972).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR25","doi-asserted-by":"publisher","first-page":"10806","DOI":"10.1074\/jbc.271.18.10806","volume":"271","author":"AM Edelman","year":"1996","unstructured":"Edelman, A.M. et al. Multiple Ca(2+)-calmodulin-dependent protein kinase kinases from rat brain. Purification, regulation by Ca(2+)-calmodulin, and partial amino acid sequence. J. Biol. Chem. 271, 10806\u201310810 (1996).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR26","doi-asserted-by":"publisher","first-page":"19320","DOI":"10.1074\/jbc.270.33.19320","volume":"270","author":"H Tokumitsu","year":"1995","unstructured":"Tokumitsu, H., Enslen, H. & Soderling, T.R. Characterization of a Ca2+\/calmodulin-dependent protein kinase cascade. Molecular cloning and expression of calcium\/calmodulin-dependent protein kinase kinase. J. Biol. Chem. 270, 19320\u201319324 (1995).","journal-title":"J. Biol. Chem."},{"key":"BFng0800_448_CR27","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1083\/jcb.137.2.263","volume":"137","author":"JC Reyes","year":"1997","unstructured":"Reyes, J.C., Muchardt, C. & Yaniv, M. Components of the human SWI\/SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J. Cell Biol. 137, 263\u2013274 (1997).","journal-title":"J. Cell Biol."}],"container-title":["Nature Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/ng0800_448.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ng0800_448","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ng0800_448.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T20:50:14Z","timestamp":1684443014000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ng0800_448"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2000,8]]},"references-count":27,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2000,8]]}},"alternative-id":["BFng0800_448"],"URL":"https:\/\/doi.org\/10.1038\/78153","relation":{},"ISSN":["1061-4036","1546-1718"],"issn-type":[{"value":"1061-4036","type":"print"},{"value":"1546-1718","type":"electronic"}],"subject":[],"published":{"date-parts":[[2000,8]]}}}