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Apoptosis in human reproductive tissues: emerging concepts

Published online by Cambridge University Press:  03 June 2009

Masao Izawa  and
John Yeh
Masao Izawa
Affiliation:
Department of Obstetrics, Gynecology, and Reproductive Biology, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass., USA Department of Biosignaling, School of Life Science, Faculty of Medicine, Tottori University, YomagoJapan
John Yeh*
Affiliation:
Department of Obstetrics, Gynecology, and Reproductive Biology, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass., USA
*
Department of Obstetrics and Gynecology, Regions Hospital, 640 Jackson St., St. Paul, MN-55101, USA
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Extract

In summary, apoptosis is an important concept in understanding many facets of human reproduction. Recent advances in the understanding of molecular mechanisms of apoptosis will allow us to understand this physiologically important process. How can the modulation of this process be applied to human reproduction? Studies to further understand the abnormalities of apoptosis, either too much or too little, may lead to a better understanding of the clinical problems in human reproduction.

We summarize future directions towards further understanding the roles of apoptotic processes in human reproduction in Table 3. The diseases listed in Table 3 are problems which could be approached from the apoptosis point of view. With further study using this concept as the lens, new diagnostic tools or therapies may be developed for these problems.

Type
Research Article
Information
Reproductive Medicine Review , Volume 6 , Issue 1 , March 1997 , pp. 23 - 36
Copyright
Copyright © Cambridge University Press 1997

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References

1Jacobson, MD, Weil, M, Raff, MC. Programmed cell death in animal development. Cell 1997; 88: 347–54.CrossRefGoogle ScholarPubMed
2Nagata, S. Apoptosis by death factor. Cell 1997; 88: 355–65.CrossRefGoogle ScholarPubMed
3Iwasaki, K, Izawa, M, Mihara, M. DNA-damageinduced apoptosis in rat skin. J Dermatol Sci 1996; 12: 31–5.CrossRefGoogle ScholarPubMed
4Iwasaki, K, Izawa, M, Mihara, M. Involvement of caspases in ultraviolet B-induced apoptosis in A431 human epitheloid tumor cells. Biochem Mol Biollnt. 1997; in press.CrossRefGoogle Scholar
5Suda, T, Takahashi, T, Golstein, P, Nagata, S. Molecular cloning and expression of the Fas ligand: a novel member of the tumor necrosis factor family. Cell 1993; 75: 1169–78.CrossRefGoogle ScholarPubMed
6Tanaka, M, Suda, T, Haze, K et al. Fas ligand in human serum. Nature Med 1996; 2: 317–22.CrossRefGoogle ScholarPubMed
7Nagata, S, Golstein, P. The Fas death factor. Science 1995; 267: 1449–56.CrossRefGoogle ScholarPubMed
8Itoh, N, Yonehara, S, Ishii, A et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991; 66: 233–43.CrossRefGoogle ScholarPubMed
9Vandenabeele, P, Declerq, W, Beyaert, R, Fiers, W. Two tumor necrosis factor receptors: structure and function. Trends Cell Biol 1995; 5: 392–9.CrossRefGoogle ScholarPubMed
10Chinnaiyan, AM, O'Rourke, K, Yu, GL et al. Signal transduction by DR-3, a death domaincontaining receptor related to TNFR-1 and CD95. Science 1996; 274: 990–2.CrossRefGoogle Scholar
11Kiston, J, Raven, T, Jiang, YP et al. A deathdomain-containing receptor that mediates apoptosis. Nature 1996; 384: 372–75.Google Scholar
12Brojatsch, J, Naughton, J, Rolls, MM, Zingler, K, Young, JAT. CAR 1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosissarcoma viruses and mediate apoptosis. Cell 1996; 87: 845–55.CrossRefGoogle Scholar
13Enari, M, Hase, A, Nagata, S. Apoptosis by a cytosolic extract from Fas-activated cells. EMBO J 1995; 14: 5201–8.CrossRefGoogle ScholarPubMed
14Enari, M, Talanian, RV, Wong, WW, Nagata, S. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 1996; 380: 723–6.CrossRefGoogle ScholarPubMed
15Izawa, M, Kato, Y, Iwasaki, K. Induction of a receptor-mediated genomic DNA fragmentation in rat thymus following administration of glucocorticoids with different biopotencies: an approach by cell-free system. Endocr J 1997; in press.CrossRefGoogle Scholar
16Kuida, K, Lippke, JA, Ku, G et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1β converting enzyme. Science 1995; 267: 2000–3.CrossRefGoogle Scholar
17Kuida, K, Zheng, TS, Na, SQ et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 1996; 384: 368–72.CrossRefGoogle ScholarPubMed
18Veis, DJ, Sorenson, CM, Shutter, JR, Korsmeyer, SJ. Bcl-2-deficient mice demonstrate fulminent lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993 75: 229–40.CrossRefGoogle Scholar
19Shimizu, S, Eguchi, Y, Kamiike, W, Matsuda, H, Tsujimoto, Y. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene 1996; 12: 2251–7.Google ScholarPubMed
20Chinnaiyan, AM, Orth, K, O'Rourke, K, Duan, H, Poirier, GG, Dixit, VM. Molecular ordering of the cell death pathway. J Biol Chem 1996; 271: 4543–76.CrossRefGoogle ScholarPubMed
21Steller, H. Mechanisms and genes of cellular suicide. Science 1995; 267: 1445–9.CrossRefGoogle ScholarPubMed
22White, E. Life, death, and the pursuit of apoptosis. Genes Dev 1996; 10: 1–15.CrossRefGoogle ScholarPubMed
23Milligan, CE, Prevette, D, Yaginuma, H et al. Peptide inhibitors for the ICE protease family arrest programmed cell death of mononeurons in vivo and in vitro. Neuron 1995; 15: 385–93.CrossRefGoogle Scholar
24Jacobson, MD, Weil, M, Raff, MC. Role of CED-3/ICE family proteases in staurosporine-induced programmed cell death. J Cell Biol 1996; 133: 1041–51.CrossRefGoogle Scholar
25Coucouvanis, E, Martin, GR. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 1995; 83: 279–84.CrossRefGoogle ScholarPubMed
26El Shershaby, AM, Hinchlitte, JR. Cell redundancy in the zona-intact preimplantation mouse blastocyst: a light and electron microscope study of dead cells and their fate. J Embryol Exp Morphol 1974 31: 643–54.Google ScholarPubMed
27Allan, DJ, Harmon, BU, Kerr, JFR. Cell death in spermatogenesis. In: Potten, CS ed. Perspectives on mammalian cell death. London: Oxford Press, 1987; 229–58.Google Scholar
28Thiet, MP, Suwanvanichkij, V, Kwok, C, Yeh, J. DAN laddering, consistent with programmed cell death, is a normal finding in human placentas. Am J Obstet Gynecol 1995; 172: 272.Google Scholar
29Nelson, DM. Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast. Placenta 1996; 17: 387–91.CrossRefGoogle ScholarPubMed
30Yasuda, M, Umemura, S, Osamura, RY, Kenjo, T, Tsutsumi, Y. Apoptotic cells in human endometrium and placental villi: pitfalls in applying the TUNEL method. Arch Histol Cytol 1995; 58: 185–90.CrossRefGoogle ScholarPubMed
31O'Shea, JD, Hay, MF, Cran, DG. Ultrastructural changes in the theca interna during follicular atresia in sheep. J Reprod Fertil 1978; 54: 183–7.CrossRefGoogle ScholarPubMed
32O'Shea, JD, Nightingale, MG, Chamley, WA. Changes in small blood vessels during cyclical luteal regression in sheep. Biol Reprod 1977; 17: 162–77.CrossRefGoogle ScholarPubMed
33Kerr, JF, Wyllie, AH, Currie, AR. Apoptosis: a basic biochemical phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239–57.CrossRefGoogle ScholarPubMed
34Hurwitz, A, Adashi, EY. Ovarian follicular atresia as an apoptotic process: a paradigm for programmed cell death in endocrine tissues. Mol Cell Endocrinol 1992; 84: C19–C23.CrossRefGoogle ScholarPubMed
35Tilly, JL, Kowalski, KI, Johnson, AL, Hsueh, AJ. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 1991; 129: 2799–801.CrossRefGoogle ScholarPubMed
36Palumbo, A, Yeh, J. In situ localization of apoptosis in the rat ovary during follicular atresia. Biol Reprod 1994; 51: 888–95.CrossRefGoogle ScholarPubMed
37Yeh, J, Lin, MC, Hasselblatt, K. Concurrent expression of fas and bcl-2 mRNA in hyperandrogenized rat granulosa cells. Mol Biol Cell 1994; 5: 95a.Google Scholar
38Tilly, JL, Tilly, KI, Kenton, ML, Johnson, AL. Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is a ssociated with decreased bax and constitutive bcl-2 and bcl-Xionß messenger ribonucleic aid levels. Endocrinology 1995; 136: 232–41.CrossRefGoogle Scholar
39Guo, MW, Mori, E, Xu, JP, Mori, T. Identification of Fas antigen associated with apoptotic cell death in murine ovary. Biochem Biophys Res Commun 1994; 203: 1438–46.CrossRefGoogle ScholarPubMed
40Quirk, SM, Cowan, RG, Joshi, SG, Henrikson, KP. Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol Reprod 1995; 52: 279–87.CrossRefGoogle ScholarPubMed
41Sanders, SL, Kaynard, AH, Melner, MH. Localization and expression of sulfated glycoprotein-2(SGP-2) mRNA in the rat ovary. [Abstract 1632]. Proceedings of the 75th Meeting of The Endocrine Society 1993.Google Scholar
42Lee, BS, Robinson, RD, Best, CL, Hill, JA, Yeh, J. Expression of apoptosis related genes, bcl-2 and TRP M-2, in human lutenized granulosa cells [Abstract]. J Soc Gynecol Invest 1995; 2: 389.Google Scholar
43Kondo, H, Maruo, T, Peng, X, Mochizuki, M. Immunological evidence for the expression of the Fas antigen in the infant and adult human ovary during follicular regression and atresia. J Clin Endocrinol Metab 1996; 81: 2702–10.Google ScholarPubMed
44Li, S, Maruo, T, Ladin-Llabe, CA, Kondo, H, Mochizuki, M. Stage-limited expression of myc oncoprotein in human ovary during follicular growth, regression and atresia. Endocrin J 1994; 41: 83–92.CrossRefGoogle ScholarPubMed
45Yeh, J, Osathanondh, R, Villa-Komaroff, L. Expression of messenger ribonucleic acid for epidermal growth factor and its ligands, epidermal growth factor and transforming growth factoralpha, in human first- and second-trimester fetal ovary and uterus. Am J Obstet Gynecol 1993; 168: 1569–73.CrossRefGoogle Scholar
46Yeh, J, Osathanondh, R. Expression of messenger ribonucleic acids encoding for basic fibroblast growth factor (FGF) and alternatively spliced FGF receptor in human fetal ovary and uterus. J Clin Endocrinol Metab 1993; 77: 1367–71.Google Scholar
47Schilling, B, Yeh, J. Messenger RNA and protein expression of transforming growth factor (TGF) β1, β2, β3 and their receptors (R1.R2) in human fetal oogenesis [Abstract O-014]. 62nd Annual Meeting of American Society for Reproductive Medicine, Boston, Mass., 2–6 11, 1996.Google Scholar
48Bennett, RA, Osathanondh, R, Yeh, J. Immunohistochemical localization of transforming growth factor-α, epidermal growth factor and EGF receptor in the human fetal ovary. J Clin Endocrinol Metab 1996; 81: 3073–6.Google ScholarPubMed
49Bennett, RA, Osthanondh, R, Yeh, J. Programmed cell death in second-trimester human fetal ovaries [Abstract P-156]. 51st Annual Meeting of American Society for Reproductive Medicine, Seatle, Wash., 7–12 10 1995.Google Scholar
50Oberhammer, FA, Pavelka, M, Sharma, S et al. Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor p 1. Proc Natl Acad Sci USA 1992; 89: 5408–12.CrossRefGoogle Scholar
51Schulze-Osthoff, K, Walczak, H, Droge, W, Krammer, H. Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 1994; 127: 15–20.CrossRefGoogle Scholar
52Jacobson, MD, Burne, J, Raff, MC. Programmed cell death and bcl-2 protein in the absence of a nucleus. EMBO J 1994; 13: 1899–910.CrossRefGoogle ScholarPubMed
53Palumbo, A, Yeh, J. In situ identification of apoptosis in a rat model of polycystic ovarian disease [Abstract 073]. Proceedings of the 41st Meeting of the Society for Gynecologic Investigation, Chicago, Ill., 22–24 03 1994.Google Scholar
54Stein, IF, Leventhal, ML. Amenorrhea associated with bilateral polycystic ovaries. Am J Obstet Gynecol 1935; 29: 181–91.CrossRefGoogle Scholar
55Almahbobi, G, Anderiesz, C, Hutchinson, P, McFarlane, JR, Wood, C, Trouson, AO. Functional integrity of granulosa cells from polycystic ovaries. Clin Endocrinol 1996; 44: 571–80.CrossRefGoogle ScholarPubMed
56Yeh, J, Kim, HH. Polycystic Ovary Syndrome (PCOS): the possible roles of apoptosis in human granulosa cells. In: Chang, RJ ed. Polycystic ovary syndrome (Serono Symposia), New York: Springer-Verlag, 1996: 51–70.CrossRefGoogle Scholar
57Palumbo, A, Yeh, J. Apoptosis as a basic mechanism in the ovarian cycle: follicular atresia and luteal regression. J Soc Gynecol Invest 1995; 2: 565–73.Google ScholarPubMed
58Lee, BS, Yeh, J. The molecular basis of follicular atresia: apoptosis as a possible mechanism. Adv Contracep Dev Sys 1996; 12: 269–82.Google Scholar
59Sheets, EE, Yeh, J. The role of apoptosis in gynecologic malignancies. Ann Med 1997; in press.CrossRefGoogle Scholar
60Sheets, EE, Crum, CP, Yeh, J. Association between cervical neoplasia and apoptosis as detected by in situ nuclear labeling. Gynecol Oncol 1996; 63: 94–100.CrossRefGoogle ScholarPubMed
61Sheets, EE, McGahan, C, Crum, CP, Yeh, J. Genetic control of apoptosis during cervical neoplasia. Gynecol Oncol 1996; 62: 417.Google Scholar
62Shoji, Y, Saegusa, M, Takano, Y, Ohbu, M, Okayasu, I. Correlation of apoptosis with tumor cell differentiation, progression, and HPV infection in cervical carcinoma. J Clin Pathol 1996; 49: 134–38.CrossRefGoogle ScholarPubMed
63Isacson, C, Kessis, TD, Hedrick, L, Cho, KR. Both cell proliferation and apoptosis increase with lesion grade in cervical neoplasia but do not correlate with human papillomavirus. Cancer Res 1996; 56: 669–74.Google Scholar
64Garzetti, GG, Ciavattini, A, Provinciali, M et al. Expression of p53 and apoptosis of tumor cells in locally advanced cervical carcinoma after cisplatin based neoadjuvant chemotherapy. Anticancer Res 1996; 16: 3229–34.Google ScholarPubMed
65Levin, EL, Renehan, A, Gossiel, R et al. Apoptosis, intrinsic readiosensitivity and prediction of radiotherapy. Radiother Oncol 1995; 37: 1–9.CrossRefGoogle Scholar
66Hughes, DE, Dai, A, Triffee, JC, Li, HH, Mundy, GR, Boyce, BF. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med 1996;2: 1132–36.CrossRefGoogle ScholarPubMed
67Isaacs, JT. Antagonistic effect of androgen on prostatic cell death. Prostate 1984; 5: 545–57.CrossRefGoogle ScholarPubMed
68Kerr, JFR, Searle, J. Deletion of cells by apoptosis during castration-induced involution of the rat prostate. Virchows Arch B 1973; 13: 87–102.Google ScholarPubMed
69Kyprianou, N, Isaacs, JT. Activation of programmed cell death in the rat ventral prostate after castration. Endocrinology 1988; 122: 552–62.CrossRefGoogle ScholarPubMed
70English, HF, Kyprianou, N, Isaacs, JT. Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration. Prostate 1989; 15: 233–50.CrossRefGoogle ScholarPubMed
71Izawa, M. Expression of sulfated glycoprotein, 2 and pSvr-1 genes and involution of steroid hormone-dependent rat tissues. Endocrinol Jpn 1991; 38: 61–6.CrossRefGoogle ScholarPubMed
72Montpetit, ML, Lawless, KR, Tenniswood, M. Androgen repressed messages in the rat ventral prostate. Prostate 1986; 8: 25–36.CrossRefGoogle ScholarPubMed
73Buttyan, R, Olsson, CA, Pinter, J et al. Induction of the TRPM-2 gene in cells undergoing programmed cell death. Mol Cell Biol 1989; 9: 3473–81.CrossRefGoogle Scholar
74Kyprianou, N, Isaacs, JT. Expression of transforming growth factor-β in the rat ventral prostate during castration-induced programmed cell death. Mol Endocrinol 1989 3: 1515–22.CrossRefGoogle ScholarPubMed
75Buttyan, R, Zakeri, Z, Lockshin, R, Wolgemuth, P. C ascade induction of c-fos, c-myc, and heat shock 70 k transcripts during regression of the rat ventral prostate gland. Mol Endocrinol 1988; 2: 650–57.CrossRefGoogle Scholar
76Quarmby, VE, Beckman, WC Jr, Wilson, EM, French, FS. Androgen regulation of c-myc messenger ribonucleic acid levels in rat ventral prostate. Mol Endocrinol 1987; 1: 856–74.CrossRefGoogle ScholarPubMed
77Izawa, M. Molecular cloning and sequencing of rat Max cDNA: castration-induced expression of the 2kb transcript in male accessory sex organs of rats. Biochim Biophys Acta 1993; 1261: 492–4.CrossRefGoogle Scholar
78Suzuki, A, Matsuzawa, A, Iguchi, T. Down regulation of Bcl-2 is the first step on Fasmediated apoptosis of male reproductive tract. Oncogene 1996; 13: 31–7.Google ScholarPubMed
79Izawa, M, Kimura, M, Saji, M. Castration-induced expression of ICE (interleukin -1β converting enzyme) in male accessory sex organs of rats. The Proceeding of Annual Meeting of Japan Society of Andrology. Workshop on Apoptosis, Kurashiki, Japan, 07 19–20, 1996.Google Scholar
80Izawa, M. Identification of a transcript predicting an alternative form of sulfated glycoprotein- 2(clusterin) in rat tissues. Biochem Mol Biol Int 1997; in press.CrossRefGoogle Scholar
81Berges, R, Furuya, Y, Remington, L, English, HF, Jacks, T, Isaacs, JT. Cell proliferation, DNA repair, and p53 function are not required for programmed cell death of prostatic glandular cells induced by androgen ablation. Proc Natl Acad Sci USA 1994; 90: 8910–14.CrossRefGoogle Scholar
82Furuya, Y, Lin, XS, Walsh, JC, Nelson, WG, Isaacs, JT. Androgen ablation-induced programmed cell death of prostatic glandular cells does not involve recruitment into a defective cell cycle or p53 induction. Endocrinology 1995; 136: 1898–906.CrossRefGoogle ScholarPubMed
83Bianco-Rodriguez, J, Martinez-Garcia, C. Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: reevaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Prolif 1996; 29: 13–31.Google Scholar
84Shetty, J, Marathe, GK, Dighe, RR. Specific immunoneutralization of FSH leads to apoptotic cell death of the pachytene spermatocytes and spermatogonical cells in the rat. Endocrinology 1996; 137: 2179–82.CrossRefGoogle ScholarPubMed
85Blanco-Rodrigez, J, Martinez-Garcia, C. Induction of apoptotic cell death in the seminiferous tubule of the adult rat testis: assessment of the germ cell types that exhibit the ability to enter apoptosis after hormone suppression by oestradiol. Int J Androl 1996; 19: 237–47.CrossRefGoogle Scholar
86Shikone, T, Billing, H, Hsueh, AJ. Experimentally induced cryptorchidism increases apoptosis in rat testis. Biol Reprod 1995; 51: 865–72.CrossRefGoogle Scholar
87Kyprianou, N, English, HF, Isaacs, JY. Programmed cell death during regression of PC-82 human prostate cancer following androgen ablation. Cancer Res 1990; 50: 3748–53.Google ScholarPubMed
88Rittmaster, RS, Norman, RW, Thomas, LN, Rowden, G. Evidence for atrophy and apoptosis in the prostates of men given finasteride. J Clin Endocrinal Metab 1996; 81: 814–819.Google ScholarPubMed
89Bauer, JJ, Sesterhenn, IA, Mostofi, FK, McLeod, DG, Srivastava, S, Moul, JW. Elevated levels of apoptosis regulator protins p53 and bcl-2 are independent prognostic biomarkers in surgically treated clinically localized prostate cancer. J Urol 1996; 156: 1511–16.CrossRefGoogle Scholar
90Magi-Galluzzi, C, Mishra, R, Fiorentino, M et al. Mitogen-activated protein kinase phophatase 1 is overexpressed in prostate cancers and is inversely related to apoptosis. Lab Invest 1997; 76: 35–51.Google Scholar
91Heiskanen, P, Billig, H, Toppari, J et al. Apoptotic cell death in the normal and cryptorchid human testis: the effect of human chorionic gonadotropin on testicular cell survival. Pediatr Res 1996; 40: 351–56.CrossRefGoogle ScholarPubMed
92Smith, CA, Williams, GT, Kingston, R, Jenkinson, EJ, Owen, JJ. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 1989; 337: 181–4.CrossRefGoogle ScholarPubMed
93Benhamou, LE, Cazenave, PA, Sarthou, P. Antiimmunoglobulins induce death by apoptosis in WEHI-231 B lymphoma cells. Eur J Immunol 1990; 20: 1405–7.CrossRefGoogle ScholarPubMed
94Sheiness, D, Bishop, JM. DNA and RNA from uninfected vertebrate cells contain nucleotide sequences related to the putative transforming gene of avian myelocytomatosis virus. J Virol 1979; 31: 514–21.CrossRefGoogle Scholar
95Lee, SY, Sugiyama, A, Sueoka, N, Kuchino, Y. Point mutation of the neu gene in rat neural tumor RT4-AC cells: suppression of tumorigenicity by s-MYC. Jpn J Cancer Res 1990; 81: 1085–8.CrossRefGoogle ScholarPubMed
96Yonshi-Rouach, E, Resnitzky, D, Lotem, J, Sachs, L, Kimchi, A, Oren, M. Wild-type p53 induces apoptosis of myeloid leukemic cells that is inhibited by interleukin-6. Nature 1991; 352: 345–47.CrossRefGoogle Scholar
97Woronicz, JD, Calnan, B, Ngo, V, Winoto, A. Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 1994; 367: 277–81.CrossRefGoogle ScholarPubMed
98Matsuzaki, Y, Fujisawa, J, Yoshida, M. Identification of transcriptional activation domain of TREB5, a CREB/ATF family protein that binds to HTLV-1 enhancer. J Biochem (Tokyo) 1995; 117: 303–8.CrossRefGoogle ScholarPubMed
99Shi, L, Nishioka, WK, Th'ng, J, Brasbury, EM, Litchfield, DW, Greenberg, AH. Premature p34cdc2 activation required for apoptosis. Science 1994; 263: 1143–5.CrossRefGoogle ScholarPubMed
100Montague, JW, Gaido, ML, Frye, C, Cidlowski, JA. A calcium-dependent nuclease from apoptotic rat thymocytes is homologous with cyclophilin. Recombinant cyclophilins A, B, and C have nuclease activity. J Biol Chem 1994; 269: 18877–80.CrossRefGoogle Scholar
101Packham, G, Cleveland, JL. Ornithine decarboxylase is a mediator of c-Myc-induced apoptosis. Mol Cell Biol 1994; 14: 5741–7.Google ScholarPubMed
102Melino, G, Annicchiarico-Petruzzelli, M, Piredda, L et al. Tissue transglutaminase and apoptosis: sense and antisense transfection studies with human neuroblastoma cells. Mol Cell Biol 1994; 14: 6584–96.Google ScholarPubMed
103Koh, JY, Yang, LL, Cotman, CW. Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res 1990; 533: 315–20.CrossRefGoogle ScholarPubMed
104Shi, L, Kraut, RP, Aebersold, R, Greenberg, AH. A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J Exp Med 1992; 175: 553–66.CrossRefGoogle ScholarPubMed
105Berke, G. The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. Ann Rev Immunol 1994; 12: 753–73.CrossRefGoogle ScholarPubMed
106Yang, E, Zha, J, Jockel, J, Boise, LH, Thompson, CB, Korsmeyer, SJ. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 1995; 80: 285–91.CrossRefGoogle ScholarPubMed
107Takayama, S, Sato, T, Krajewski, S et al. Cloning and functional analysis of BAG-1: a novel Bcl-2- binding protein with anti-cell death activity. Cell 1995; 80: 279–84.CrossRefGoogle ScholarPubMed
108Boyd, JM, Gallo, GJ, Elangovan, B et al. Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survivalpromoting proteins. Oncogene 1995; 11: 1921–8.Google Scholar
109Chittenden, T, Harrington, EA, O'Conner, R et al. Induction of apoptosis by Bcl-2 homolog Bak. Nature 1995; 374: 733–6.CrossRefGoogle ScholarPubMed
110Kiefer, MC, Brauer, MJ, Powers, VC et al. Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 1995; 374: 736–9.CrossRefGoogle ScholarPubMed
111Boyd, JM, Malstrom, S, Subramanian, T et al. Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 1994; 79: 341–51.CrossRefGoogle Scholar
112Lin, EY, Orlofsky, A, Berger, MS, Prystowsky, MB. Characterization of Al, a novel hemopoieticspecific early-response gene with sequence similarity to bcl-2. J Immunol 1993; 151: 1978–88.CrossRefGoogle Scholar
113Kozopas, KM, Yang, T, Buchan, HL, Zhou, P, Craig, RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 1993; 90: 3516–20.CrossRefGoogle ScholarPubMed
114Opipari, AW Jr, Hu, HM, Yabkowitz, R, Dixit, VM. The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J Biol Chem 1992; 267: 12424–7.CrossRefGoogle ScholarPubMed
115Sugawara, S, Takeda, K, Lee, A, Dennert, G. Suppression of stress protein GRP78 induction in tumor B/C10ME eliminates resistance to cell mediated cytotoxicity. Cancer Res 1993; 53: 6001–5.Google ScholarPubMed
116Nakashima, T, Sekiguchi, T, Kuraoka, A et al. Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells. Mol Cell Biol 1993; 13: 6367–74.Google ScholarPubMed
117Fath, I, Schweighoffer, F, Rey, I et al. Cloning of a Grb2 isoform with apoptotic properties. Science 1994; 264: 971–4.CrossRefGoogle ScholarPubMed
118Wong, GH, Elwell, JH, Oberley, LW, Goeddel, DV. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 1989; 58: 923–31.CrossRefGoogle ScholarPubMed
119Rosen, DR, Siddique, T, Patterson, D et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993; 362: 59–62.CrossRefGoogle ScholarPubMed
120Hockenbery, DM, Oltvai, ZN, Yin, XM, Milliam, CL, Korsmeyer, SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993;75: 241–51.CrossRefGoogle Scholar
121Ishida, Y, Agata, Y, Shibahara, K, Honjo, T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J 1992; 11: 3887–95.CrossRefGoogle ScholarPubMed
122Owens, GP, Hahn, WE, Cohen, JJ. Identification of mRNA associated with programmed cell death in immature thymocytes. Mol Cell Biol 1991; 11: 77–88.Google ScholarPubMed
123Dowd, DR, MacDonald, PN, Komm, BS, Haussler, MR, Miesfeld, R. Evidence for early induction of calmodulin in gene expression in lymphocytes undergoing glucocorticoid-mediated apoptosis. J Biol Chem 1991; 266: 18423–6.CrossRefGoogle ScholarPubMed
124Alnemri, ES, Livingston, DJ, Niclholson, DW et al. Human ICE/CED-3 protease nomenclature. Cell 1996; 87: 171.CrossRefGoogle ScholarPubMed