1,522
Views
25
CrossRef citations to date
0
Altmetric
Review

New insights into germ cell migration and survival/apoptosis in spermatogenesis

Lessons from CD147

, , &
Pages 264-272 | Published online: 01 Dec 2012

References

  • Toyama Y, Maekawa M, Yuasa S. Ectoplasmic specializations in the Sertoli cell: new vistas based on genetic defects and testicular toxicology. Anat Sci Int 2003; 78:1 - 16; http://dx.doi.org/10.1046/j.0022-7722.2003.00034.x; PMID: 12680465
  • Wong EW, Mruk DD, Cheng CY. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim Biophys Acta 2008; 1778:692 - 708; http://dx.doi.org/10.1016/j.bbamem.2007.11.006; PMID: 18068662
  • Yan HH, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or a foe of spermatogenesis?. Bioessays 2007; 29:36 - 48; http://dx.doi.org/10.1002/bies.20513; PMID: 17187371
  • Yan W, Samson M, Jégou B, Toppari J. Bcl-w forms complexes with Bax and Bak, and elevated ratios of Bax/Bcl-w and Bak/Bcl-w correspond to spermatogonial and spermatocyte apoptosis in the testis. Mol Endocrinol 2000; 14:682 - 99; http://dx.doi.org/10.1210/me.14.5.682; PMID: 10809232
  • Chang IY, Kim JH, Park KH, Yoon SP. Experimental varicocele induces p53-dependent germ cell apoptosis through activation of γ-H2AX. Urol Int 2010; 85:216 - 20; http://dx.doi.org/10.1159/000316356; PMID: 20530960
  • Matulis S, Handel MA. Spermatocyte responses in vitro to induced DNA damage. Mol Reprod Dev 2006; 73:1061 - 72; http://dx.doi.org/10.1002/mrd.20508; PMID: 16700071
  • Aitken RJ, Findlay JK, Hutt KJ, Kerr JB. Apoptosis in the germ line. Reproduction 2011; 141:139 - 50; http://dx.doi.org/10.1530/REP-10-0232; PMID: 21148286
  • Wang J, Gu H, Lin H, Chi T. Essential roles of the chromatin remodeling factor BRG1 in spermatogenesis in mice. Biol Reprod 2012; 86:186; http://dx.doi.org/10.1095/biolreprod.111.097097; PMID: 22495890
  • Lee NP, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: is this a potential target for male contraceptive development?. Hum Reprod Update 2004; 10:349 - 69; http://dx.doi.org/10.1093/humupd/dmh026; PMID: 15192055
  • Yan HH, Mruk DD, Lee WM, Cheng CY. Cross-talk between tight and anchoring junctions-lesson from the testis. Adv Exp Med Biol 2008; 636:234 - 54; http://dx.doi.org/10.1007/978-0-387-09597-4_13; PMID: 19856171
  • Cheng CY, Wong EW, Yan HH, Mruk DD. Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol Cell Endocrinol 2010; 315:49 - 56; http://dx.doi.org/10.1016/j.mce.2009.08.004; PMID: 19682538
  • Iacono KT, Brown AL, Greene MI, Saouaf SJ. CD147 immunoglobulin superfamily receptor function and role in pathology. Exp Mol Pathol 2007; 83:283 - 95; http://dx.doi.org/10.1016/j.yexmp.2007.08.014; PMID: 17945211
  • Kirk P, Wilson MC, Heddle C, Brown MH, Barclay AN, Halestrap AP. CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J 2000; 19:3896 - 904; http://dx.doi.org/10.1093/emboj/19.15.3896; PMID: 10921872
  • Shirozu M, Tada H, Tashiro K, Nakamura T, Lopez ND, Nazarea M, et al. Characterization of novel secreted and membrane proteins isolated by the signal sequence trap method. Genomics 1996; 37:273 - 80; http://dx.doi.org/10.1006/geno.1996.0560; PMID: 8938438
  • Vitiello A, Sette A, Yuan L, Farness P, Southwood S, Sidney J, et al. Comparison of cytotoxic T lymphocyte responses induced by peptide or DNA immunization: implications on immunogenicity and immunodominance. Eur J Immunol 1997; 27:671 - 8; http://dx.doi.org/10.1002/eji.1830270315; PMID: 9079808
  • Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 1996; 56:5309 - 18; PMID: 8968075
  • Sun J, Hemler ME. Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res 2001; 61:2276 - 81; PMID: 11280798
  • Tang W, Chang SB, Hemler ME. Links between CD147 function, glycosylation, and caveolin-1. Mol Biol Cell 2004; 15:4043 - 50; http://dx.doi.org/10.1091/mbc.E04-05-0402; PMID: 15201341
  • Weidle UH, Scheuer W, Eggle D, Klostermann S, Stockinger H. Cancer-related issues of CD147. Cancer Genomics Proteomics 2010; 7:157 - 69; PMID: 20551248
  • Juel C, Halestrap AP. Lactate transport in skeletal muscle - role and regulation of the monocarboxylate transporter. J Physiol 1999; 517:633 - 42; http://dx.doi.org/10.1111/j.1469-7793.1999.0633s.x; PMID: 10358105
  • Kanyenda LJ, Verdile G, Boulos S, Krishnaswamy S, Taddei K, Meloni BP, et al. The dynamics of CD147 in Alzheimer’s disease development and pathology. J Alzheimers Dis 2011; 26:593 - 605; PMID: 21694447
  • Ochrietor JD, Linser PJ. 5A11/Basigin gene products are necessary for proper maturation and function of the retina. Dev Neurosci 2004; 26:380 - 7; http://dx.doi.org/10.1159/000082280; PMID: 15855767
  • Sameshima T, Nabeshima K, Toole BP, Yokogami K, Okada Y, Goya T, et al. Expression of emmprin (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas. Int J Cancer 2000; 88:21 - 7; http://dx.doi.org/10.1002/1097-0215(20001001)88:1<21::AID-IJC4>3.0.CO;2-S; PMID: 10962435
  • Polette M, Gilles C, Marchand V, Lorenzato M, Toole B, Tournier JM, et al. Tumor collagenase stimulatory factor (TCSF) expression and localization in human lung and breast cancers. J Histochem Cytochem 1997; 45:703 - 9; http://dx.doi.org/10.1177/002215549704500508; PMID: 9154157
  • Abraham D, Zins K, Sioud M, Lucas T, Aharinejad S. Host CD147 blockade by small interfering RNAs suppresses growth of human colon cancer xenografts. Front Biosci 2008; 13:5571 - 9; http://dx.doi.org/10.2741/3100; PMID: 18508606
  • Lecona E, Olmo N, Turnay J, Santiago-Gómez A, López de Silanes I, Gorospe M, et al. Kinetic analysis of butyrate transport in human colon adenocarcinoma cells reveals two different carrier-mediated mechanisms. Biochem J 2008; 409:311 - 20; http://dx.doi.org/10.1042/BJ20070374; PMID: 17760565
  • Muraoka K, Nabeshima K, Murayama T, Biswas C, Koono M. Enhanced expression of a tumor-cell-derived collagenase-stimulatory factor in urothelial carcinoma: its usefulness as a tumor marker for bladder cancers. Int J Cancer 1993; 55:19 - 26; http://dx.doi.org/10.1002/ijc.2910550105; PMID: 8344748
  • Jiang JL, Zhou Q, Yu MK, Ho LS, Chen ZN, Chan HC. The involvement of HAb18G/CD147 in regulation of store-operated calcium entry and metastasis of human hepatoma cells. J Biol Chem 2001; 276:46870 - 7; http://dx.doi.org/10.1074/jbc.M108291200; PMID: 11591720
  • Li Y, Xu J, Chen L, Zhong WD, Zhang Z, Mi L, et al. HAb18G (CD147), a cancer-associated biomarker and its role in cancer detection. Histopathology 2009; 54:677 - 87; http://dx.doi.org/10.1111/j.1365-2559.2009.03280.x; PMID: 19438743
  • Pepper MS. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 2001; 21:1104 - 17; http://dx.doi.org/10.1161/hq0701.093685; PMID: 11451738
  • Biswas C. Tumor cell stimulation of collagenase production by fibroblasts. Biochem Biophys Res Commun 1982; 109:1026 - 34; http://dx.doi.org/10.1016/0006-291X(82)92042-3; PMID: 6297481
  • Lim M, Martinez T, Jablons D, Cameron R, Guo H, Toole B, et al. Tumor-derived EMMPRIN (extracellular matrix metalloproteinase inducer) stimulates collagenase transcription through MAPK p38. FEBS Lett 1998; 441:88 - 92; http://dx.doi.org/10.1016/S0014-5793(98)01474-4; PMID: 9877171
  • Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H, et al. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 1995; 55:434 - 9; PMID: 7812975
  • Guo H, Zucker S, Gordon MK, Toole BP, Biswas C. Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J Biol Chem 1997; 272:24 - 7; http://dx.doi.org/10.1074/jbc.272.1.24; PMID: 8995219
  • Gabison EE, Hoang-Xuan T, Mauviel A, Menashi S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie 2005; 87:361 - 8; http://dx.doi.org/10.1016/j.biochi.2004.09.023; PMID: 15781323
  • Dai JY, Dou KF, Wang CH, Zhao P, Lau WB, Tao L, et al. The interaction of HAb18G/CD147 with integrin alpha6beta1 and its implications for the invasion potential of human hepatoma cells. BMC Cancer 2009; 9:337; http://dx.doi.org/10.1186/1471-2407-9-337; PMID: 19775453
  • Curtin KD, Meinertzhagen IA, Wyman RJ. Basigin (EMMPRIN/CD147) interacts with integrin to affect cellular architecture. J Cell Sci 2005; 118:2649 - 60; http://dx.doi.org/10.1242/jcs.02408; PMID: 15928045
  • Li Y, Wu J, Song F, Tang J, Wang SJ, Yu XL, et al. Extracellular membrane-proximal domain of HAb18G/CD147 binds to metal ion-dependent adhesion site (MIDAS) motif of integrin β1 to modulate malignant properties of hepatoma cells. J Biol Chem 2012; 287:4759 - 72; http://dx.doi.org/10.1074/jbc.M111.277699; PMID: 22130661
  • Tang J, Wu YM, Zhao P, Yang XM, Jiang JL, Chen ZN. Overexpression of HAb18G/CD147 promotes invasion and metastasis via alpha3beta1 integrin mediated FAK-paxillin and FAK-PI3K-Ca2+ pathways. Cell Mol Life Sci 2008; 65:2933 - 42; http://dx.doi.org/10.1007/s00018-008-8315-8; PMID: 18695939
  • Wu YM, Tang J, Zhao P, Chen ZN, Jiang JL. Enhanced expression of Hab18g/CD147 and activation of integrin pathway in HCC cells under 3-D co-culture conditions. Cell Biol Int 2009; 33:199 - 206; http://dx.doi.org/10.1016/j.cellbi.2008.11.006; PMID: 19059491
  • Lescaille G, Menashi S, Cavelier-Balloy B, Khayati F, Quemener C, Podgorniak MP, et al. EMMPRIN/CD147 up-regulates urokinase-type plasminogen activator: implications in oral tumor progression. BMC Cancer 2012; 12:115; http://dx.doi.org/10.1186/1471-2407-12-115; PMID: 22443116
  • Zhao P, Zhang W, Wang SJ, Yu XL, Tang J, Huang W, et al. HAb18G/CD147 promotes cell motility by regulating annexin II-activated RhoA and Rac1 signaling pathways in hepatocellular carcinoma cells. Hepatology 2011; 54:2012 - 24; http://dx.doi.org/10.1002/hep.24592; PMID: 21809360
  • Wu J, Ru NY, Zhang Y, Li Y, Wei D, Ren Z, et al. HAb18G/CD147 promotes epithelial-mesenchymal transition through TGF-β signaling and is transcriptionally regulated by Slug. Oncogene 2011; 30:4410 - 27; http://dx.doi.org/10.1038/onc.2011.149; PMID: 21532623
  • Smedts AM, Curry TE Jr.. Expression of basigin, an inducer of matrix metalloproteinases, in the rat ovary. Biol Reprod 2005; 73:80 - 7; http://dx.doi.org/10.1095/biolreprod.104.036145; PMID: 15758150
  • Kuno N, Kadomatsu K, Fan QW, Hagihara M, Senda T, Mizutani S, et al. Female sterility in mice lacking the basigin gene, which encodes a transmembrane glycoprotein belonging to the immunoglobulin superfamily. FEBS Lett 1998; 425:191 - 4; http://dx.doi.org/10.1016/S0014-5793(98)00213-0; PMID: 9559645
  • Xiao LJ, Chang H, Ding NZ, Ni H, Kadomatsu K, Yang ZM. Basigin expression and hormonal regulation in mouse uterus during the peri-implantation period. Mol Reprod Dev 2002; 63:47 - 54; http://dx.doi.org/10.1002/mrd.10128; PMID: 12211060
  • Noguchi Y, Sato T, Hirata M, Hara T, Ohama K, Ito A. Identification and characterization of extracellular matrix metalloproteinase inducer in human endometrium during the menstrual cycle in vivo and in vitro. J Clin Endocrinol Metab 2003; 88:6063 - 72; http://dx.doi.org/10.1210/jc.2003-030457; PMID: 14671212
  • Li W, Alfaidy N, Challis JR. Expression of extracellular matrix metalloproteinase inducer in human placenta and fetal membranes at term labor. J Clin Endocrinol Metab 2004; 89:2897 - 904; http://dx.doi.org/10.1210/jc.2003-032048; PMID: 15181074
  • Igakura T, Kadomatsu K, Kaname T, Muramatsu H, Fan QW, Miyauchi T, et al. A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev Biol 1998; 194:152 - 65; http://dx.doi.org/10.1006/dbio.1997.8819; PMID: 9501026
  • Chen H, Fok KL, Yu S, Jiang J, Chen Z, Gui Y, et al. CD147 is required for matrix metalloproteinases-2 production and germ cell migration during spermatogenesis. Mol Hum Reprod 2011; 17:405 - 14; http://dx.doi.org/10.1093/molehr/gar013; PMID: 21343160
  • Maekawa M, Suzuki-Toyota F, Toyama Y, Kadomatsu K, Hagihara M, Kuno N, et al. Stage-specific localization of basigin, a member of the immunoglobulin superfamily, during mouse spermatogenesis. Arch Histol Cytol 1998; 61:405 - 15; http://dx.doi.org/10.1679/aohc.61.405; PMID: 9990424
  • Saxena DK, Oh-Oka T, Kadomatsu K, Muramatsu T, Toshimori K. Behaviour of a sperm surface transmembrane glycoprotein basigin during epididymal maturation and its role in fertilization in mice. Reproduction 2002; 123:435 - 44; http://dx.doi.org/10.1530/rep.0.1230435; PMID: 11882021
  • Toyama Y, Maekawa M, Kadomatsu K, Miyauchi T, Muramatsu T, Yuasa S. Histological characterization of defective spermatogenesis in mice lacking the basigin gene. Anat Histol Embryol 1999; 28:205 - 13; http://dx.doi.org/10.1046/j.1439-0264.1999.00194.x; PMID: 10458027
  • Saxena DK, Toshimori K. Molecular modifications of MC31/CE9, a sperm surface molecule, during sperm capacitation and the acrosome reaction in the rat: is MC31/CE9 required for fertilization?. Biol Reprod 2004; 70:993 - 1000; http://dx.doi.org/10.1095/biolreprod.103.021667; PMID: 14645104
  • Siu MK, Cheng CY. Extracellular matrix: recent advances on its role in junction dynamics in the seminiferous epithelium during spermatogenesis. Biol Reprod 2004; 71:375 - 91; http://dx.doi.org/10.1095/biolreprod.104.028225; PMID: 15115723
  • Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A, et al. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod 2005; 72:985 - 91; http://dx.doi.org/10.1095/biolreprod.104.036400; PMID: 15601913
  • Kanatsu-Shinohara M, Takehashi M, Takashima S, Lee J, Morimoto H, Chuma S, et al. Homing of mouse spermatogonial stem cells to germline niche depends on beta1-integrin. Cell Stem Cell 2008; 3:533 - 42; http://dx.doi.org/10.1016/j.stem.2008.08.002; PMID: 18983968
  • Overall CM. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002; 22:51 - 86; http://dx.doi.org/10.1385/MB:22:1:051; PMID: 12353914
  • Amălinei C, Căruntu ID, Bălan RA. Biology of metalloproteinases. Rom J Morphol Embryol 2007; 48:323 - 34; PMID: 18060181
  • Nuttall RK, Sampieri CL, Pennington CJ, Gill SE, Schultz GA, Edwards DR. Expression analysis of the entire MMP and TIMP gene families during mouse tissue development. FEBS Lett 2004; 563:129 - 34; http://dx.doi.org/10.1016/S0014-5793(04)00281-9; PMID: 15063736
  • Wong CH, Cheng CY. The blood-testis barrier: its biology, regulation, and physiological role in spermatogenesis. Curr Top Dev Biol 2005; 71:263 - 96; http://dx.doi.org/10.1016/S0070-2153(05)71008-5; PMID: 16344108
  • Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 2010; 6:380 - 95; http://dx.doi.org/10.1038/nrendo.2010.71; PMID: 20571538
  • Cheng CY, Mruk DD. An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective. Crit Rev Biochem Mol Biol 2009; 44:245 - 63; http://dx.doi.org/10.1080/10409230903061207; PMID: 19622063
  • Yan HH, Mruk DD, Wong EW, Lee WM, Cheng CY. An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008; 105:8950 - 5; http://dx.doi.org/10.1073/pnas.0711264105; PMID: 18579774
  • Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the beta1 integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945 - 64; http://dx.doi.org/10.1095/biolreprod.103.023606; PMID: 14645107
  • Yan HH, Mruk DD, Cheng CY. Junction restructuring and spermatogenesis: the biology, regulation, and implication in male contraceptive development. Curr Top Dev Biol 2008; 80:57 - 92; http://dx.doi.org/10.1016/S0070-2153(07)80002-0; PMID: 17950372
  • Xia W, Mruk DD, Lee WM, Cheng CY. Differential interactions between transforming growth factor-beta3/TbetaR1, TAB1, and CD2AP disrupt blood-testis barrier and Sertoli-germ cell adhesion. J Biol Chem 2006; 281:16799 - 813; http://dx.doi.org/10.1074/jbc.M601618200; PMID: 16617054
  • Nahalkova J, Volkmann I, Aoki M, Winblad B, Bogdanovic N, Tjernberg LO, et al. CD147, a gamma-secretase associated protein is upregulated in Alzheimer’s disease brain and its cellular trafficking is affected by presenilin-2. Neurochem Int 2010; 56:67 - 76; http://dx.doi.org/10.1016/j.neuint.2009.09.003; PMID: 19751784
  • Gu J, Zhang C, Chen R, Pan J, Wang Y, Ming M, et al. Clinical implications and prognostic value of EMMPRIN/CD147 and MMP2 expression in pediatric gliomas. Eur J Pediatr 2009; 168:705 - 10; http://dx.doi.org/10.1007/s00431-008-0828-5; PMID: 18795327
  • Zhu C, Pan Y, He B, Wang B, Xu Y, Qu L, et al. Inhibition of CD147 gene expression via RNA interference reduces tumor cell invasion, tumorigenicity and increases chemosensitivity to cisplatin in laryngeal carcinoma Hep2 cells. Oncol Rep 2011; 25:425 - 32; PMID: 21165561
  • Wang B, Xu YF, He BS, Pan YQ, Zhang LR, Zhu C, et al. RNAi-mediated silencing of CD147 inhibits tumor cell proliferation, invasion and increases chemosensitivity to cisplatin in SGC7901 cells in vitro. J Exp Clin Cancer Res 2010; 29:61; http://dx.doi.org/10.1186/1756-9966-29-61; PMID: 20525232
  • Abraham D, Zins K, Sioud M, Lucas T, Aharinejad S. Host CD147 blockade by small interfering RNAs suppresses growth of human colon cancer xenografts. Front Biosci 2008; 13:5571 - 9; http://dx.doi.org/10.2741/3100; PMID: 18508606
  • Hou Q, Tang X, Liu H, Tang J, Yang Y, Jing X, et al. Berberine induces cell death in human hepatoma cells in vitro by downregulating CD147. Cancer Sci 2011; 102:1287 - 92; http://dx.doi.org/10.1111/j.1349-7006.2011.01933.x; PMID: 21443647
  • Dean NR, Knowles JA, Helman EE, Aldridge JC, Carroll WR, Magnuson JS, et al. Anti-EMMPRIN antibody treatment of head and neck squamous cell carcinoma in an ex-vivo model. Anticancer Drugs 2010; 21:861 - 7; http://dx.doi.org/10.1097/CAD.0b013e32833d1a11; PMID: 20700044
  • Kuang YH, Chen X, Su J, Wu LS, Liao LQ, Li D, et al. RNA interference targeting the CD147 induces apoptosis of multi-drug resistant cancer cells related to XIAP depletion. Cancer Lett 2009; 276:189 - 95; http://dx.doi.org/10.1016/j.canlet.2008.11.010; PMID: 19097686
  • Baba M, Inoue M, Itoh K, Nishizawa Y. Blocking CD147 induces cell death in cancer cells through impairment of glycolytic energy metabolism. Biochem Biophys Res Commun 2008; 374:111 - 6; http://dx.doi.org/10.1016/j.bbrc.2008.06.122; PMID: 18616931
  • Intasai N, Mai S, Kasinrerk W, Tayapiwatana C. Binding of multivalent CD147 phage induces apoptosis of U937 cells. Int Immunol 2006; 18:1159 - 69; http://dx.doi.org/10.1093/intimm/dxl050; PMID: 16740601
  • Tang J, Guo YS, Zhang Y, Yu XL, Li L, Huang W, et al. CD147 induces UPR to inhibit apoptosis and chemosensitivity by increasing the transcription of Bip in hepatocellular carcinoma. Cell Death Differ 2012; http://dx.doi.org/10.1038/cdd.2012.60; PMID: 22595757
  • Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, et al. transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab 2007; 92:3292 - 304; http://dx.doi.org/10.1210/jc.2007-0367; PMID: 17504903
  • Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: regulation and biology. Philos Trans R Soc Lond B Biol Sci 2010; 365:1501 - 15; http://dx.doi.org/10.1098/rstb.2009.0124; PMID: 20403866
  • Martinvalet D, Zhu P, Lieberman J. Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis. Immunity 2005; 22:355 - 70; http://dx.doi.org/10.1016/j.immuni.2005.02.004; PMID: 15780992
  • Fridman JS, Lowe SW. Control of apoptosis by p53. Oncogene 2003; 22:9030 - 40; http://dx.doi.org/10.1038/sj.onc.1207116; PMID: 14663481
  • Fauvet R, Dufournet C, Poncelet C, Uzan C, Hugol D, Daraï E. Expression of pro-apoptotic (p53, p21, bax, bak and fas) and anti-apoptotic (bcl-2 and bcl-x) proteins in serous versus mucinous borderline ovarian tumours. J Surg Oncol 2005; 92:337 - 43; http://dx.doi.org/10.1002/jso.20424; PMID: 16299808
  • Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 2006; 281:7260 - 70; http://dx.doi.org/10.1074/jbc.M509868200; PMID: 16407291
  • Yu J, Zhang L. The transcriptional targets of p53 in apoptosis control. Biochem Biophys Res Commun 2005; 331:851 - 8; http://dx.doi.org/10.1016/j.bbrc.2005.03.189; PMID: 15865941
  • Ihrie RA, Bronson RT, Attardi LD. Adult mice lacking the p53/p63 target gene Perp are not predisposed to spontaneous tumorigenesis but display features of ectodermal dysplasia syndromes. Cell Death Differ 2006; 13:1614 - 8; http://dx.doi.org/10.1038/sj.cdd.4401871; PMID: 16485031
  • Burns TF, Bernhard EJ, El-Deiry WS. Tissue specific expression of p53 target genes suggests a key role for KILLER/DR5 in p53-dependent apoptosis in vivo. Oncogene 2001; 20:4601 - 12; http://dx.doi.org/10.1038/sj.onc.1204484; PMID: 11498783
  • Coates PJ. p53 and Mdm2: not all cells are equal. J Pathol 2007; 213:357 - 9; http://dx.doi.org/10.1002/path.2275; PMID: 17973240
  • Chen H, Fok KL, Jiang X, Jiang J, Chen Z, Gui Y, et al. CD147 regulates apoptosis in mouse spermatocytes but not spermatogonia. Hum Reprod 2012; 27:1568 - 76; http://dx.doi.org/10.1093/humrep/des050; PMID: 22451502
  • Blanco-Rodríguez J. A matter of death and life: the significance of germ cell death during spermatogenesis. Int J Androl 1998; 21:236 - 48; http://dx.doi.org/10.1046/j.1365-2605.1998.00133.x; PMID: 9805237