The immunomodulatory protein SV-IV protects serum-deprived cells against apoptosis but not against G0/G1 arrest: Possible implications for the survival of implanting embryo

Journal of Cellular Physiology

Volumn 212, Issue 3, 2007, Pages 610-625

  Morelli, Francesco ^a   Peluso, Gianfranco ^b   Petillo, Orsolina ^b   Giannattasio, Angela ^a   Filosa, Silvana ^c   Motta, Chiara M ^c   Tammaro, Stefania ^c   Zatterale, Adriana ^d   Calzone, Rita ^d   Budillon, Alfredo ^e   Cartenì, Maria ^c   De Maria, Salvatore ^c   Costanza, Maria R ^c   Nigro, Antonella ^c   Petrazzuolo, Marcella ^c   Buommino, Elisabetta ^a   Rizzo, Maria ^c   Capasso, Giovanni ^c   Baiano, Salvatore ^a   Moscatiello, Francesco ^a   Ravagnan, Gianpietro ^f   Fuggetta, Maria P ^b   Tajana, Gianfranco ^g   Stiuso, Paola ^c   Metafora, Bianca M ^a   Metafora, Vittoria ^a   Metafora, Salvatore ^a   more..

^a INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d Ospedale Elena d'Aosta   (Italy)

^e NATIONAL CANCER INSTITUTE   (Italy)

^f CA' FOSCARI UNIVERSITY OF VENICE   (Italy)

^g UNIVERSITY OF SALERNO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CATALASE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLOOXYGENASE 1; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; INHIBITOR OF APOPTOSIS PROTEIN; MESSENGER RNA; MYC PROTEIN; PROTEIN BAX; PROTEIN C FOS; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; RETINOBLASTOMA PROTEIN; SEMINAL VESICLE PROTEIN IV; SURVIVIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL MEMBRANE; CELL PROTECTION; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOBLASTOID CELL; MALE; MOUSE; NIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAJI CELL; SURVIVAL;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CATALASE; CELL LINE, TUMOR; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; CYCLIN-DEPENDENT KINASES; CYCLINS; CYTOTOXICITY, IMMUNOLOGIC; DNA FRAGMENTATION; EMBRYO CULTURE TECHNIQUES; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; G0 PHASE; G1 PHASE; GENOMIC INSTABILITY; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED BALB C; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; SEMINAL VESICLE SECRETORY PROTEINS; SERUM; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 34547932436     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21058     Document Type: Article

References (82)

1. Abrescia P, Lombardi G, De Rosa M, Quagliozzi L, Guardiola J, Metafora S. 1985. Identification and preliminary characterization of a sperm-binding protein in normal human semen. J Reprod Fertil 73:71-77.
2. Bai J, Cederbaum AI. 2003. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents by accelerating the degradation of p53. J Biol Chem 278:4660-4667.
3. Battistuzzi G, D'Urso M, Toniolo D, Persico GM, Luzzatto L. 1985. Tissue-specific levels of human glucose-6-phosphate dehydrogenase correlate with methylation of specific sites at the 3′ end of the gene. Proc Natl Acad Sci USA 82:1465-1469.
4. Bredesen DE, Mehlen P, Rabizadeh S. 2005. Receptors that mediate cellular dependence. Cell Death Differ 12:1031-1043.
5. Browett PJ, Norton JD. 1989. Analysis of ras gene mutations and methylation state in human leukemias. Oncogene 4:1029-1036.
6. Camussi G, Tetta C, Bussolino F, Metafora S, Peluso G, Esposito C, Porta R. 1990. An anti-inflammatory protein secreted from the rat seminal vesicle epithelium inhibits the synthesis of platelet-activating factorand the release of arachidonic acid and prostacyclin. Eur J Biochem 192:481-485.
7. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
8. Cocchiara R, Lampiasi N, Albeggiani G, Azzolina A, Bongiovanni A, Gianaroli L, Di Blasi F, Geraci D. 1996. A factor secreted by human embryo stimulates cytokine release by uterine mast cell. Mol Hum Reprod 2:781-791.
9. D'Ambrosio E, Del Grosso N, Ravagnan G, Peluso G, Metafora S. 1993. Cloning and expression of the rat genomic DNA sequence coding for the secreted form of the protein SV-IV. Bull Mol Biol Med 18:215-223.
10. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H. 2004. Molecular cues to implantation. Endocr Rev 25:341-373.
11. Drissi R, Zindy F, Roussel MF, Cleveland JL. 2001. c-Myc-mediated regulation of telomerase activity is disabled in immortalized cells. J Biol Chem 276:29994-30001.
12. Droge W. 2002. Free radicals in the physiological control of cell function. Physiol Rev 82:47-95.
13. Esposito C, Cozzolino A, Porta R, Mariniello L, Buommino E, Morelli F, Metafora V, Metafora S. 2002. Protein SV-IV promotes nitric oxide production not associated with apoptosis in murine macrophages. Eur J Cell Biol 81:185-196.
14. Esterbauer H, Cheeseman KH. 1990. Determination of aldehyde lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407-421.
15. Fell HB, Robison R. 1929. The growth, development and phophatase activity of embryonic avian femora and limb buds cultivated in vitro. Biochem J 23:767-778.
16. Galdiero F, Tufano MA, De Martino L, Capasso C, Porta R, Ravagnan G, Peluso G, Metafora S. 1989. Inhibition of macrophage phagocytic activity by SV-IV, a major protein secreted from the rat seminal vesicle epithelium. J Reprod Immunol 16:269-284.
17. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G. 2001. Heat-shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286:433-442.
18. Goldman M. 1968. Labeling agents and procedures for conjugation. In: Fluorescent Antibody Methods. New York and London: Academic Press. pp 97-107.
19. Gordon JR, Galli SJ. 1994. Promotion of mouse fibroblast collagen gene expression by mast cells stimulated via the Fc epsilon RI. Role for mast cell-derived transforming growth factor beta and tumor necrosis factor alpha. J Exp Med 180:2027-2037.
20. Granville DJ, Gottlieb RA. 2002. Mitochondrial respiratory control is lost during growth factor deprivation. Proc Natl Acad Sci USA 99:12801-12806.
21. Guerin P, El Mouatassim S, Menezo Y. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7:175-189.
22. Hansson M, Hermodsson S, Brune M, Mellqvist UH, Naredi P, Betten A, Gehlsen KR, Hellstrand K. 1999. Histamine protects T cells and natural killer cells against oxidative stress. J Interferon Cytokine Res 19:1135-1144.
23. Hao ZM, Luo JY, Cheng J, Li L, He D, Wang QY, Yang GX. 2005. Intensive inhibition of hTERT expression by a ribozyme induces rapid apoptosis of cancer cells through a telomere length-independent pathway. Cancer Biol Ther 4:1098-1103.
24. Harris SE, Mansson PE, Tully DB, Burkhart B. 1983. Seminal vesicle secretion IV gene: allelic difference due to a series of 20-base-pair direct tandem repeats within an intron. Proc Natl Acad Sci USA 80:6460-6464.
25. Islam KN, Kayanoki Y, Kaneto H, Suzuki K, Asahi M, Fujii J, Taniguchi N. 1997. TGF-beta1 triggers oxidative modifications and enhances apoptosis in HIT cells through accumulation of reactive oxygen species by suppression of catalase and glutathione peroxidase. Free Radic Biol Med 22:1007-1017.
26. Krysan K, Dalwadi H, Sharma S, Pold M, Dubinett S. 2004a. Cyclooxygenase 2-dependent expression of survivin is critical for apoptosis resistance in non-small cell lung cancer. Cancer Res 64:6359-6362.
27. Krysan K, Merchant FH, Zhu L, Dohadwala M, Luo J, Lin Y, Heuze-Vourc'h N, Pold MD, Seligson D, Chia D, Goodglick L, Wang H, Strieter R, Sharma S, Dubinett S. 2004b. COX-2-dependent stabilization of survivin in non-small cell lung cancer. FASEB J 18:206-208.
28. Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, Marchisio PC, Altieri DC. 1998. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396:580-584.
29. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA, Robinson JP. 2003. DPI induces mitochondrial superoxide-mediated apoptosis. Free Radic Biol Med 34:465-477.
30. Lieberthal W, Triaca V, Koh JS, Pagano PJ, Levine JS. 1998. Role of superoxide in apoptosis induced by growth factor withdrawal. Am J Physiol 275:F691-F702.
31. Lin CK, Kalunta CI, Chen FS, Nguyen TT, Kaptein JS, Lad PM. 1995. Dimethyl sulfoxide suppresses apoptosis in Burkitt's lymphoma cells. Exp Cell Res 216:403-410.
32. Liptay S, Fulda S, Schanbacher M, Bourteele S, Ferri KF, Kroemer G, Adler G, Debatin KM, Schmid RM. 2002. Molecular mechanisms of sulfasalazine-induced T-cell apoptosis. Br J Pharmacol 137:608-620.
33. Lu LF, Lind EF, Gondek DC, Bennett KA, Gleeson MW, Pino-Lagos K, Scott ZA, Coyle AJ, Reed JL, Van Snick J, Strom TB, Zheng XX, Noelle RJ. 2006. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442:997-1002.
34. MacGlashan D Jr. 2003. Histamine: a mediator of inflammation. J Allergy Clin Immunol 112:S53-S59.
35. Mansson PE, Sugino A, Harris SE. 1981. Use of a cloned double stranded cDNA coding for a major androgen dependent protein in rat seminal vesicle secretion: the effect of testosterone in gene expression. Nucleic Acids Res 9:935-946.
36. Massey WA, Guo CB, Dvorak AM, Hubbard WC, Bhagavan BS, Cohan VL, Warner JA, Kagey-Sobotka A, Lichtenstein LM. 1991. Human uterine mast cells. Isolation, purification, characterization, ultrastructure, and pharmacology. J Immunol 147:1621-1627.
37. McConkey DJ, Orrenius S. 1996. Signal transduction pathways in apoptosis. Stem Cells 14:619-631.
38. Mellqvist UH, Hansson M, Brune M, Dahlgren C, Hermodsson S, Hellstrand K. 2000. Natural killer cell dysfunction and apoptosis induced by chronic myelogenous leukemia cells: role of reactive oxygen species and regulation by histamine. Blood 96:1961-1968.
39. Metafora S, Facchiano F, Facchiano A, Esposito C, Peluso G, Porta R. 1987. Homology between rabbit uteroglobin and the rat seminal vesicle sperm binding protein: prediction of structural features of glutamine substrates for transglutaminase. J Protein Chem 6:353-6359.
40. Metafora S, Peluso G, Persico P, Ravagnan G, Esposito C, Porta R. 1989a. Immunosuppressive and anti-inflammatory properties of a major protein secreted from the epithelium of the rat seminal vesicles. Biochem Pharmacol 38:121-131.
41. Metafora S, Porta R, Ravagnan G, Peluso G, Tufano MA, De Martino L, Ianniello R, Galdiero F. 1989b. Inhibitory effect of SV-IV, a major protein secreted from the rat seminal vesicle epithelium, on phagocytosis and chemotaxis of human polymorphonuclear leukocytes. J Leukocyte Biol 46:409-416.
42. Metafora V, Franco P, Massa O, Morelli F, Stiuso P, Ferranti P, Mamone G, Malorni A, Stoppelli MP, Metafora S. 2001. Phosphorylation of seminal vesicle protein IV on Ser58 enhances its peroxidase-stimulating activity. Eur J Biochem 268:3858-3869.
43. Michimata T, Tsuda H, Sakai M, Fujimura M, Nagata K, Nakamura M, Saito S. 2002. Accumulation of CRTH2-positive T-helper 2 and T-cytotoxic 2 cells at implantation sites of human decidua in a prostaglandin D(2)-mediated manner. Mol Hum Reprod 8:181-187.
44. Miele L, Cordella-Miele E, Mukherjee AB. 1987. Uteroglobin: structure, molecular biology, and new perspectives on its function as a phospholipase A2 inhibitor. Endocr Rev 8:474-490.
45. Millbacher A, King NJC. 1989. Target cell lysis by natural killer cells is influenced by beta 2-microglobulin expression. Scand J Immunol 30:21-29.
46. Moretta L, Moretta A. 2004. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 23:255-259.
47. Mosser DD, Caron AW, Bourget L, Meriin AB, Sherman MY, Morimoto RI, Massie B. 2000. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20:7146-7159.
48. Mukherjee AB, Kundu GC, Mantile-Selvaggi G, Yuan CJ, Mandal AK, Chattopadhyay S, Zheng F, Pattabiraman N, Zhang Z. 1999. Uteroglobin: a novel cytokine! Cell Mol Life Sci 55:771-787.
49. Nakagawa Y. 2004. Role of mitochondrial phospholipid hydroperoxide glutathione peroxidase (PHGPx) as an antiapoptotic factor. Biol Pharm Bull 27:956-960.
50. Ostrowski MC, Kistler MK, Kistler WS. 1979. Purification and cell-free synthesis of a major protein from rat seminal vesicle secretion. A potential marker for androgen action. J Biol Chem 254:383-390.
51. Pan YC, Li SSL. 1982. Structure of secretory protein IV from rat seminal vesicles. Int J Pept Protein Res 20:177-187.
52. Pandey S, Lopez C, Jammu A. 2003. Oxidative stress and activation of proteasome protease during serum deprivation-induced apoptosis in rat hepatoma cells; inhibition of cell death by melatonin. Apoptosis 8:497-508.
53. Paonessa G, Metafora S, Tajana G, Abrescia P, De Santis A, Gentile V, Porta R. 1984. Transglutaminase-mediated modifications of the rat sperm surface in vitro. Science 226:852-555.
54. Park SS, Kim JS, Tessarollo L, Owens JD, Peng L, Han SS, Tae Chung S, Torrey TA, Cheung WC, Polakiewicz RD, McNeil N, Ried T, Mushinski JF, Morse HC 3rd, Janz S. 2005. Insertion of c-Myc into Igh induces B-cell and plasma-cell neoplasms in mice. Cancer Res 65:1306-1315.
55. Peluso G, Porta R, Esposito C, Tufano MA, Toraldo R, Vuotto ML, Ravagnan G, Metafora S. 1994. Suppression of rat epididymal sperm immunogenicity by a seminal vesicle secretory protein and transglutaminase both in vivo and in vitro. Biol Reprod 50:593-602.
56. Peluso G, Marchese M, Russo Spena S, Furgi A, Ranieri M, Ravagnan G, Fuggetta MP, Porta R, Metafora V, Metafora S. 1997. SV-IV, a major protein secreted from rat seminal vesicle epithelium, promotes lymphocyte cytotoxic activity against the lymphoblastoid Raji cell line in human peripheral blood mononuclear cells. Int J Cancer 72:321-328.
57. Pentland AP, Scott G, VanBuskirk J, Tanck C, LaRossa G, Brouxhon S. 2004. Cyclooxygenase-I deletion enhances apoptosis but does not protect against ultraviolet light-induced tumors. Cancer Res 64:5587-5591.
58. Perham P. 2004. NK cells and throphoblasts: partners in pregnancy. J Exp Med 200:951-955.
59. Porta R, Esposito C, Metafora S, Malorni A, Pucci P, Siciliano R, Marino G. 1991. Mass spectrometric identification of the amino donor and acceptor sites in a transglutaminase protein substrate secreted from rat seminal vesicles. Biochemistry 30:3114-3120.
60. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO. 2006. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol 4: 1, e9 0070-0086.
61. Reynolds JL, Akhter J, Adams WJ, Morris DL. 1997. Histamine content in colorectal cancer. Are there sufficient levels of histamine to affect lymphocyte function? Eur J Surg Oncol 23:224-227.
62. Romano-Carratelli C, Galdiero M, Nuzzo I, Bentivoglio C, Porta R, Peluso G, Ravagnan G, Metafora S. 1995. In vivo inhibition of cell-mediated and humoral immune responses to cellular antigens by SV-IV, a major protein secreted from the rat seminal vesicle epithelium. J Reprod Immunol 28:15-30.
63. Romano-Carratelli C, Bentivoglio C, Nuzzo I, Benedetto N, Buommino E, Cozzolino A, Carteni M, Morelli F, Costanza MR, Metafora B, Metafora V, Metafora S. 2002. Effect of protein SV-IV on experimental Salmonella enterica serovar Typhimurium infection in mice. Clin Diagn Lab Immunol 9:115-125.
64. Rouass-Freis N, Marchal-Bras Goncalves R, Menier C, Dausset J, Carosella ED. 1997. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci USA 94:11520-11525.
65. Samuels BL, Murray JL, Cohen MB, Safe AR, Sinha BK, Townsend AJ, Beckett MA, Weichselbaum RR. 1991. Increased glutathione peroxidase activity in ahuman sarcoma cell line with inherent doxorubicin resistance. Cancer Res 51:521-527.
66. Santagada V, Ialenti A, Metafora S, Caliendo G, Maffia P, Morelli F, De Rosa R, De Maria S, Carteni M. 2002. Anti-inflammatory peptides: an update and future perspectives. Recent Res Devel Peptides 1:1-33.
67. Seru R, Mondola P, Damiano S, Svegliati S, Agnese S, Avvedimento EV, Santillo M. 2004. HaRas activates the NADPH oxidase complex in human neuroblastoma cells via extracellular signal-regulated kinase 1/2 pathway. J Neurochem 91:613-622.
68. Stiuso P, Metafora S, Facchiano AM, Colonna G, Ragone R. 1999. The self-association of protein SV-IV and its possible functional implications. Eur J Biochem 266:1029-1035.
69. Sun Y, Tang XM, Half E, Kuo MT, Sinicrope FA. 2002. Cyclooxygenase-2 overexpression reduces apoptotic susceptibility by inhibiting the cytochrome c-dependent apoptotic pathway in human colon cancer cells. Cancer Res 62:6323-6328.
70. Takayama S, Xie Z, Reed JC. 1999. An evolutionary conserved family of Hsp70/Hsc70 molecular chaperone regulators. J Biol Chem 274:781-786.
71. Thompson EB. 1998. The many roles of c-myc in apoptosis. Annu Rev Physiol 60: 575-600.
72. Tian WN, Pignatare JN, Stanton RC. 1994. Signal transduction proteins that associate with the platelet-derived growth factor (PDGF) receptor mediate the PDGF-induced release of glucose-6-phosphate dehydrogenase from permeabilized cells. J Biol Chem 269:14798-14805.
73. Tian WN, Braunstein LD, Apse K, Pang J, Rose M, Tian X, Stanton RC. 1999. Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am J Physiol 276:C1121-C1131.
74. Tufano MA, Porta R, Farzati B, Di Pierro P, Rossano F, Catalanotti P, Baroni A, Metafora S. 1996. Rat seminal vesicle protein SV-IV and its transglutaminase-synthesized polyaminated derivative SPD2-SV-IV induce cytokine release from human resting lymphocytes and monocytes in vitro. Cell Immunol 168:148-157.
75. Urosevic M, Dummer R. 2002. HLA-G - An ace up the sleeve? ASHI Quarterly 26:106-109.
76. van den Heuvel MJ, Xie X, Tayade C, Peralta C, Fang Y, Leonard S, Paffaro VA Jr, Sheikhi AK, Murrant C, Croy BA. 2005. A review of trafficking and activation of uterine natural killer cells. Am J Reprod Immunol 54:322-331.
77. Vuotto ML, Peluso G, Mancino D, Colonna G, Facchiano A, Ielpo MT, Ravagnan G, Metafora S. 1993. Inhibition of interleukin-1 release and activity by the rat seminal vesicle protein SV-IV. J Leukoc Biol 53:214-222.
78. Wang J, Xie LY, Allan S, Beach D, Hannon GJ. 1998. Myc activates telomerase. Genes Dev 12:1769-1774.
79. Wheatley SP, McNeish IA. 2005. Survivin: a protein with dual roles in mitosis and apoptosis. Int Rev Cytol 247:35-58.
80. Wun T, McKnight H, Tuscano JM. 2004. Increased cyclooxygenase-2 (COX-2): a potential role in the pathogenesis of lymphoma. Leuk Res 28:179-190.
81. Zenclussen AC. 2006. Regulatory T cells in pregnancy. Springer Semin Immunopathol 28:31-39.
82. Zenclussen AC, Gerlof K, Zenclussen ML, Ritschel S, Zambon Bertoja A, Fest S, Hontsu S, Ueha S, Matsushima K, Leber J, Volk HD. 2006. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur J Immunol 36:82-94.