Mechanisms of hormone and growth factor action in the bovine corpus luteum

Theriogenology

Volumn 45, Issue 7, 1996, Pages 1351-1380

  Davis, J S ^a,b,c   May, J V ^a   Keel, B A ^a  

^a Dept of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE WICHITA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Growth factors; Hormone action; Map kinase; Phospholipase C; Protein kinases; Second messengers

Indexed keywords

BOVINAE;

EID: 0000774662     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/0093-691X(96)00101-X     Document Type: Article

References (135)

1. Ackland JF, Schwartz NB, Mayo KE, Dodson RE. Nonsteroidal signals originating in the gonads. Physiol Rev 1992;72:731-787.
2. Aharoni D, Dantes A, Amsterdam A. Cross-talk between adenylate cyclase activation and tyrosine phosphorylation leads to modulation of the actin cytoskeleton and to acute progestrone secretion in ovarian granulosa cells. Endocrinology 1993;133:1432-1436.
3. Bano Y, Okano Y, Nozawa Y. Thrombin-mediated phosphoinositide hydrolysis in chinese hamster ovary cells overexpressing phospholipase Cδ-1. J Biol Chem 1994;269:15846-15852.
4. Beebe SJ. The cAMP-dependent protein kinases and cAMP signal transduction. Cancer Biol 1994;5:285-294.
5. 2α. Endocrine 1996(in press).
6. Birnbaumer L. Receptor-to-effector signaling through G proteins: Roles for βγ dimers as well as α subunits. Cell 1992;71:1069-1072.
7. Bousfield GR, Perry WM, Ward DN. Gonadotropins. Chemistry and biosynthesis. In: Knobil E, Neil JD (eds). The Physiology of Reproduction, 2nd edn. New York: Raven Press, Ltd., 1994;1749-1792.
8. Budnik LT, Mukhopadhyay AK. Desensitization of LH-stimulated cyclic AMP accumulation in isolated bovine luteal cells - effect of phorbol ester. Mol Cell Endocrinol 1987;54:51-61.
9. Budnik LT, Mukhopadhyay AK. Epidermal growth factor, a modulator of luteal adenylate cyclase. J Biol Chem 1991;266(21)13908-13913.
10. Budnik LT, Mukhopadhyay AK. Phospholipase D treatment enhances gonadotropin receptor-coupled adenylate cyclase activity in isolated bovine luteal cells. FEBS 1993;326:222-226.
11. Carr DW, DeManno DA, Atwood A, Hunzicker-Dunn M, Scott JD. Follicle-stimulating hormone regulation of A-kinase anchoring proteins in granulosa cells. J Biol Chem 1993;268:20729-20732.
12. Chakravorty A, Joslyn MI, Davis JS. Characterization of insulin and insulin-like growth factor-I actions in the bovine luteal cell: regulation of receptor tyroskine kinase activity, phosphatidylinositol-3-kinase, and deoxyribonucleic acid synthesis. Endocrinology 1993; 3:1331-1340.
13. Chakravorty A, Joslyn M, Davis JS. Modulation of insulin-like growth factor (IGF-I) receptor tyrosine kinase by protein kinase A (PKA) and protein kinase C (PKC) in bovine luteal cells. Sci Prog Abstr SGI 1993:235 abstr.
14. Chakravorty A, Imakawa K, Davis JS. The aberrant tyrosine kinase negative EGF receptor in bovine luteal cells: evidence for activation of alternative signalling mechanisms. Biol Reprod 1993;48(Suppl 1):181 abstr.
15. Chegini N, Lei ZM, Rao CV, Hansel W. Cellular distribution and cycle phase dependency of gonadotropin and eicosanoid binding sites in bovine corpora lutea. Biol Reprod 1991;45:506-513.
16. Claesson-Welsh L. Platelet-derived growth factor receptor signals. J Biol Chem 1994;269:32023-32026.
17. Clark MR, Kawai Y, Davis JS, LeMaire WJ. Ovarian protein kinases. In: Toft DO, Ryan RJ (eds). Proceedings of the Fifth Ovarian Workshop. Illinois:Ovarian Workshops, 1984;383-401.
18. Cobb MH, Goldsmith EJ. How MAP kinases are regulated. J Biol Chem 1995;270:14843-14846.
19. 2+-sensitive adenylyl cyclases. Cell Signal 1994;6:823-840.
20. Cutler RE, Maizels ET, Hunzicker-Dunn M. δ Protein kinase-C in the rat ovary: estrogen regulation and localization. Endocrinology 1994;135:1669-1678.
21. Daum G, Eisenmann-Tappe I, Fries H-W, Troppmair J, Rapp UR. The ins and outs of raf kinase. TIBS 1994;19:474-480.
22. 3/DAG intracellular signalling systems in bovine luteal cells. In: Gibori G (ed). VIII Ovarian Workshop: Signaling Mechanisms and Gene Expression in the Ovary. New York: Springer Verlag, 1991;39-53.
23. Davis JS. Modulation of luteinizing homone-stimulated inositol phosphate accumulation by phorbol esters in bovine luteal cells. Endocrinology 1992;131:749-757.
24. 2α on inositol phospholipid hydrolysis in the large and small cells of the bovine corpus luteum. Mol Cell Endocrinol 1988;58:43-50.
25. 2α. J Steroid Biochem 1989,32:643-649.
26. Davis JS, Farese RV, Marsh JM. Stimulation of phospholipid labeling and steroidogenesis by luteinizing hormone in isolated bovine luteal cells. Endocrinology 1981:109:469-475.
27. Davis JS, Gangrade BK, Westfall S, Joslyn M, Chakravorty A, Mau Y-H, May JV. Growth factor receptor and tyrosine kinase and phospholipase activation in porcine theca and granulosa cells: Cell specific actions of EGF and PDGF. Scientific Program and Abstracts Society for Gynecologic Investigation 1994;100.
28. Davis JS, Khan SA, May JV. Prostaglandin F2α (PGF2α) stimulates transforming growth factor-β (TGF-β) secretion by large luteal cells: evidence for the involvement of protein kinase C. American Fertility Society 1994;S73:O-150 abstr.
29. 2α and mediation by protein kinase C and mitogen-activated protein (MAP) kinase. Biol Reprod 1995;52(Suppl 1):96 abstr.
30. 2+ in isolated bovine luteal cells. J Biol Chem 1987;262:8515-8521.
31. 2+ in bovine luteal cells. Proc Natl Acad Sci USA 1987;84:3728-3732.
32. 2+ intracellular signalling system in bovine luteal cells. FEBS 1986;208:287-291.
33. Davis RJ. MAPKs: new JNK expands the group. TIBS 1994;19:470-473.
34. Demano DA, Hunzicker-Dunn M. cAMP-dependent protein kinase isozymes in porcine follicles and corpora lutea. Mol Cell Endocrinol 1991;80:91-104.
35. 2α luteinizing hormone, and estradiol on second messenger systems and on the secretion of oxytocin and progesterone from granulosa and early luteal cells of the ewe. Biol Reprod 1994;50:765-773.
36. Dhanasekarn N, Heasley LE, Johnson GL. G rotein-coupled receptor systems involved in cell growth and oncogenesis. Endocr Rev 1995;16.259-270.
37. 2α stimulates inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate formation in bovine luteal cells. Endocrinology 1991;128:1519-1526.
38. Exton JH. Phosphatidylcholine breakdown and signal transduction. Biochim Biophys Acta 1994;1212:26-42.
39. Flores JA, Veldhuis JD. Single cell studies of the calcium second messenger signaling pathways in ovarian granulosa cells. In: Adashi EY, Leung PCK (eds). The Ovary. New York: Raven Press, Ltd., 1993;129-146.
40. Fong H, Imakawa K, Davis JS. Detection and quantification of mRNAs for the conventional class of protein kinase C isoforms (cPKC α, β, γ) in the bovine corpus luteum: regulation by PGF2α and phorbol esters. Biol Reprod 1995;52(Suppl 1):113 abstr.
41. 2-binding proteins involved in signaling by tyrosine kinase. J Biol Chem 1994;269:1518-1522.
42. Gangrade BK, Gotcher ED, Davis JS, May JV. The secretion of transforming growth factor-beta by bovine luteal cells in vitro. Mol Cell Endocrinol 1993;93:117-123.
43. Garverick HA, Smith MF, Elmore RG, Morehouse GL, Agudo LS, Zahler WL. Changes and interrelationships among luteal LH receptors, adenylate cyclase activity and phosphodiestrase activity during the bovine estrous cycle. J Anim Sci 1985;61:216-223.
44. Gille H, Strahl T, Shaw PE. Activation of ternary complex factor Elk-1 by stress-activated protein kinases. Curr Biol 1995;5:1191-1200.
45. Girsh E, Greber Y, Meidan R. Luteotrophic and luteolytic interactions between bovine small and large luteal-like cells and endothelial cells. Biol Reprod 1995;52:954-962.
46. 2+ mobilization. J Biol Chem 1992;267:4479-4488.
47. 2α treatment of ewes. Endocrine 1995;3:585-589.
48. Hansel W, Alila HW, Dowd JP, Milvae RA. Differential origin and control mechanisms in small and large bovine luteal cells. J Reprod Fertil 1991; Suppl 43:77-89.
49. Heldin C-H. Dimerization of cell surface receptors in signal transduction. Cell 1995;80:213-223.
50. Heller RA, Kronke M. Tumor necrosis factor receptor-mediated signaling pathways. J Cell Biol 1994;126:5-9.
51. Hill CS, Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 1995;80:199-211.
52. Hipkin RW, Sanchez-Yague J, Ascoli M. Agonist-induced phosphorylation of the luteinizing hormone/chorionic gonadotropin receptor expressed in a stably transfected cell line. Mol Endocrinol 1993;7:823-832.
53. 2α. Endocrinology 1992;131:743-748.
54. Hubbard CJ. EGF modulates phosphoinositide levels in ovarian granulosa cells stimulated by luteinizing hormone. J Cell Physiol 1994;160:227-232.
55. Ihle JN. Cytokine receptor signalling. Nature 1995;377:591-594.
56. Iniguez-Lluhi J, Kleuss C, Gilman AG. The importance of G-Protein βγ subunits. Trends in Cell Biol 1993;3:230-235.
57. 2α, PGE, and luteinizing hormone. Prostaglandins 1991;41:495-500.
58. 397 is important for receptor activation. J Biol Chem 1993;268:20851-20854.
59. Joslyn MI, Chakravorty A, Davis JS. Transforming growth factor beta (TGFβ) modulates DNA synthesis in cultured bovine luteal cells. Biol Reprod 1992;46(Suppl 1):151 abstr.
60. Joslyn MI, Chakravorty A, Westfall SD, Khan SA, Davis JS. Platelet-derived growth factor stimulates DNA synthesis and phospholipase C activity in bovine luteal cells. Biol Reprod 1994;50(Suppl 1):137 abstr.
61. Juengel JL, Meberg BM, Turzillo AM, Nett TM, Niswender GD. Hormonal regulation of messenger ribonucleic acid encoding steroidogenic acute regulatory protein in ovine corpora lutea. Endocrinology 1995;136:5423-5429.
62. Keel BA, Hildebrandt JM, May JV, Davis JS. Effects of epidermal growth factor on the tyrosine phosphorylation of mitogen-activated protein kinases in monolayer cultures of porcine granulosa cells. Endocrinology 1995;136:1197-1204.
63. Karin M, Hunter T. Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr Biol 1995;5:747-757.
64. Kawabe J-I, Iwani G, Ebina T, Ohno S, Katada T, Ueda Y, Homey CJ, Ishikawa Y. Differential activation of adenylyl cyclase by protein kinase C isoenzymes. J Biol Chem 1994;269:16554-16558.
65. Kawate N, Menon KMJ. Palmitoylation of luteinizing hormone/human choriogonadotropin receptors in transfected cells. J Biol Chem 1994;269:30651-30658.
66. Khan I, Hossain A, Whitman GF, Sarkar NH, McDonough PG. Differential induction of c-jun expression by PGF2-alpha in rat ovary, uterus and adrenal. Prostaglandins 1993;46:139-144.
67. Khan SA, Joslyn MI, Westfall SD, Davis JS. Characterization of protein kinase C (PKC) isoforms in bovine corpus luteum. Biol Reprod 1994;50(Suppl 1):83 abstr.
68. Lalli E, Sassone-Corsi P. Signal transduction and gene regulation: the nuclear response to cAMP. J Biol Chem 1994;269:17359-17362.
69. Lambeth JD. Receptor-regulated phospholipases and their generation of lipid mediators, which activate protein kinase C. In: Kuo JF (ed). Protein Kinase C. New York: Oxford University Press, 1994;121-161.
70. Lamm MLG, Ekstrom RC, Maizels ET, Rajagopalan RM, Hunzicker-Dunn M. The effect of protein kinases on desensitization of the porcine follicular membrane luteinizing hormone/chorionic gonadotropin-sensitive adenylyl cyclase. Endocrinology 1994;134:1745-1754.
71. Lamm MLG, Hunzicker-Dunn M. Phosphorylation-independent desensitization of the luteinizing hormone/chorionic gonadotropin receptor in porcine follicular membranes. Mol Endocrinol 1994;8:1537-1546.
72. 2 hydrolysis and regulation of phospholipase C isozymes. Curr Opin Cell Biol 1995;7:183-189.
73. LeRoith D, Werner H, Deitner-Johnson D, Roberts CT. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 1995;16:143-163.
74. Li W, Mischak H, Yu J-C, Wang L-M, Mushinski JF, Heidaran MA, Pierce JH. Tyrosine phosphorylation of protein kinase C-δ in response to its activation. J Biol Chem 1994; 269:2349-2352.
75. Liu X, Davis D, Segaloff DL. Disruption of potential sites for N-linked glycosylation does not impair hormone binding to the lutropin/choriogonadotropin receptor if Asn-173 is left intact. J Biol Chem 1993;268:1513-1516.
76. Mahoney CW, Huang K-P. Molecular and catalytic properties of protein kinase C. In: Kuo JF (ed). Protein Kinase C. New York: Oxford University Press, 1994;16-63.
77. 2+-independent lipid-stimulated kinase in the rabbit corpus luteum of pseudopregnancy. J Biol Chem 1992;267:17061-17068.
78. Majercik M, Czerwiec FS, Puett D. Effects of hormones and intracellular mediators on differentiated functions of cultured leydig tumor cells. Steroids 1989;54:627-645.
79. Malarkey K, Belham CM, Paul A, Graham A, McLees A, Scott PH. The regulation of tyrosine kinase signalling pathways by growth factor and G-protein-coupled receptors. J Biochem 1995;309:361-375.
80. Marsh JM. The stimulatory effect of luteinizing hormone on adenyl cyclase in the bovine corpus luteum. J Biol Chem 1970;245:1596-1603.
81. Marsh JM. The role of cyclic AMP in gonadal function. Adv Cyclic Nucleotide Res 1975;6:137-199.
82. Marsh JM, Savard K. The activation of luteal phosphorylase by luteinizing hormone. J Biol Chem 1964;239:1-7.
83. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995;80:179-185.
84. May JV, Schomberg DW. The potential relevance of epidermal growth factor and transforming growth factor-alpha to ovarian physiology. Seminars in Reproductive Biology 1989;7:1-11.
85. May JV, Stephenson LA, Mau Y-H, Davis JS. Central role for protein kinase C (PKC) in the regulation of porcine granulosa cells in vitro. Mol Biol Cell 1995;6(Suppl):239a abstr.
86. May JV, Turczynski CJ, Ramos L, Mau Y-H. Differential involvement of protein kinase C in the regulation of transforming growth factor-β (TGF-β) secretion by porcine theca and granulosa cells in vitro. Endocrinology 1995;136:1319-1322.
87. 2α in the ovine corpus luteum in vivo. Biol Reprod 1994;51:800-806.
88. Misrahi M, Hai MTV, Ghinea N, Loosfelt H, Meduri G, Atger M, Jolivet A, Gross B, Savouret JF, Dessen P, Milgrom E. Molecular and cellular biology of gonadotropin receptors. In: Adashi EY, Leung PCK (eds). The Ovary. New York: Raven Press, Ltd., 1993;57-92.
89. 2 in microdialyzed bovine corpus luteum in vitro. Biol Reprod 1993;49:423-430.
90. Miyamoto A, Okuda K. Schweigert FJ, Schams D. Effects of basic fibroblast growth factor, transforming growth factor-β and nerve growth factor on the secretory function of the bovine corpus luteum in vitro. Endocrinology 1992;135:103-114.
91. Miyazaki S. Inositol trisphosphate receptor mediated spatiotemporal calcium signalling. Curr Opin Cell Biol 1995;7:190-196.
92. Mochly-Rosen D. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 1995;268:247-251.
93. Moss J, Vaughan M. Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J Biol Chem 1995; 270:12327-12330.
94. Nakanishi H, Brewer KA, Exton JH. Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1993;268:13-16.
95. Newton AC. Protein kinase C: structure, function, and regulation. J Biol Chem 1995;270:28495-28498.
96. Niswender GD, Nett TM. Corpus luteum and its control in infraprimate species. In: Knobil E, Neil JD (eds). The Physiology of Reproduction, 2nd edn. New York: Raven Press, Ltd., 1994;1749-1792.
97. Owrig KE, Betrand JE, Ou B-R, Forsberg NE, Stormshak F. Immunochemical characterization and cellular distribution of protein kinase C isozymes in the bovine corpus luteum. Comp Biochem Physiol 1994;108B(1):53-57.
98. 2α-induced oxytocin secretion from the bovine corpus luteum. Endocrinology 1994;134:78-83.
99. Pawson T. Protein modules and signalling networks. Nature 1995;373:573-580.
100. Perks CM, Denning-Kendall PA, Gilmour RS, Wathes DC. Localization of messenger ribonucleic acids for insulin-like growth factor I (IGF-I), IGF-II, the type 1 IGF receptor in the ovine ovary throughout the estrous cycle. Endocrinology 1995;136:5266-5273.
101. Quest AFG, Bell RM. The molecular mechanism of protein kinase C regulation by lipids. In: Kuo JF (ed). Protein Kinase C. New York: Oxford University Press, 1994;65-95.
102. 2+ influx, and protein kinase C activation in sustained cellular responses. Endocr Rev 1995;16:649-681.
103. Reynolds LP, Grazul-Bilska AT, Killilea SD, Redmer DA. Mitogenic factors of corpora lutea. Prog Growth Factor Res 1994;5:159-175.
104. Richards, JS. Hormonal control of gene expression in the ovary. Endocr Rev 1994;15:725-751.
105. Rittenhouse SE. Regulation of phosphatidylinositide 3-kinase, a potential signaling enzyme in platelets. Sem Hematol 1995;32:120-125.
106. Roberts AB, Kim S-J, Kondaiah P, Jakowlew SB, Denhez F, Glick AB, Geiser AG, Wantanabe S, Noma T, Lechleider R, Sporn MB. Transcriptional control of expression of the TGF-βs. Ann NY Acad Sci 1990;593:43-50.
107. Ross EM. Palmitoylation in G-protein signaling pathways. Curr Biol 1995;5:107-109.
108. Sakamoto K, Miwa K, Ezashi T, Okuda-Ashitaka E, Okuda K, Houtani T, Sugimoto T, Ito S, Hayaishi O. Expression of mRNA encoding the prostaglandin F2α receptor in bovine corpora lutea throughout the oestrous cycle and pregnancy. J Reprod Fertil 1995;103:99-105.
109. Sauerwein H, Miyamoto A, Günther J, Meyer HHD, Schams D. Binding and action of insulin-like growth factors and insulin in bovine luteal tissue during the oestrous cycle. J Reprod Fertil 1992;96:103-115.
110. Scott JD, McCartney S. Localization of a-kinase through anchoring proteins. Mol Endocrinol 1994;8:5-11.
111. Segaloff DL, Ascoli M. The lutropin/choriogonadotropin receptor...4 years later. Endocr Rev 1993;14:324-347.
112. Shimamoto T, Yamoto M, Nakano R. Possible involvement of protein kinase C in gonadotropin-induced ovulation in the rat ovary. Endocrinology 1993;133:2127-2132.
113. Spaulding SW. The ways in which hormones change cyclic adenosine 3′,5′-monophosphate-dependent protein kinase subunits, and how such changes affect cell behavior. Endocr Rev 1993;14:632-650.
114. Steele GL, Leung PCK. Signal transduction mechanisms in ovarian cells. In: Adashi EY, Leung PCK (eds). The Ovary. New York: Raven Press, Ltd., 1993;113-127.
115. Stormshak F, Orwig KE, Bertrand JE. Dynamics of molecular mechanisms underlying ovarian oxytocin secretion. J Reprod Fertil 1995;Suppl 49:379-390.
116. Stoyanov B, Volinia S, Hanck T, Rubio I, Loubtchenkov M, Malek D, Stoyanova S, Vanhaesebroeck B, Dhand R, Nürnberg B, Gierschik P, Seedorf K, Hsuan JJ, Waterfield MD, Wetzker R. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 1995;269:690-693.
117. Taussig R, Gilman AG. Mammalian membrane-bound adenylyl cyclases. J Biol Chem 1995;270:1-4.
118. Tilly JL. Ovarian follicular atresia: a model to study the mechanisms of physiological cell death. Endocrine 1993;1:67-72.
119. 3. J Biol Chem 1994;269:32358-32367.
120. 2α initiates polyphosphatidylinositol hydrolysis and membrane translocation of protein kinase C in swine ovarian cells. Biochem Biophys Res Comm 1987; 149:112-117.
121. Vlodavsky I, Brown KD, Gospodarowicz D. A comparison of the binding of epidermal growth factor to cultured granulosa and luteal cells. J Biol Chem 1978;253:3744-3750.
122. 2+-dependent intracellular pathway in NIH-3T3 cells. J Biol Chem 1994;269:17619-17625.
123. ras-GTP complex and mitogen-activated protein kinase in NIH-3T3 cells via Gq-protein-coupled pathway. J Biol Chem 1995;270:8984-8990.
124. Watson AJ, Katz A, Simon MI. A fifth member of the mammalian G-protein β-subunit family. J Biol Chem 1994;269:22150-22156.
125. West LA, Weakland LL, Duncan RA, Davis JS. Dual activation of adenylate cyclase and phospholipase C by prostaglandins of E and I series in bovine luteal cells. In: Hirshfield A (ed). VII Ovarian Workshop: Paracrine Communication in the Ovary Oncogenesis and Growth Factors. New York:Plenum Publishing Co., 1989;369-374.
126. Westfall SD, Joslyn MI, Mau Y-H, May JV, Davis JS. LH stimulates phospholipase C activity in cultured porcine granulosa and theca cells. Biol Reprod 1994;50(Suppl 1):137 abstr.
127. 2α on signal transduction pathways in ovine small and large luteal cells. Biol Reprod 1995;52(Suppl 1):109 abstr.
128. Wheeler MB, Veldhuis JD. Facultative actions of the protein kinase-C effector system on hormonally stimulated adenosine 3′,5′-monophosphate production by swine luteal cells. Endocrinology 1989;125:2414-2420.
129. Wilson CJ, Applebury ML. Arresting G-protein coupled receptor activity. Curr Biol 1993;3:683-686.
130. 2α receptors in the early bovine corpus luteum. Biol Reprod 1995;52:74-78.
131. Würthner JU, Kistler M, Kratzmeier, Mukhopadhyay AK. LH/hCG-receptor is coupled to both adenylate cyclase and protein kinase C signaling pathways in isolated mouse Leydig cells. Endocrine 1995;3:579-584.
132. Yano K, Saji M, Hidaka A, Moriya N, Okuno A, Kohn LD, Cutler GB. A new constitutively activating point mutation in the luteinizing hormone/choriogonadotropin receptor gene in cases of male-limited precocious puberty. J Clin Endocrinol Metabol 1995;80:1162-1168.
133. Yao R, Cooper GM. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 1995;267:2003-2007.
134. Yoshimura M, Cooper DMF. Type-specific stimulation of adenylyl cyclase by protein kinase C. J Biol Chem 1993;268:4604-4607.
135. Zhu X, Gudermann T, Bimbaumer M, Bimbaumer L. Luteinizing hormone receptor with a severely truncated cytoplasmic tail (LHR-ct628) desensitizes to the same degree as the full-length receptor. J Biol Chem 1993;268:1723-1728.