The multi PDZ domain protein MUPP1 as a putative scaffolding protein for organizing signaling complexes in the acrosome of mammalian spermatozoa

Journal of Andrology

Volumn 27, Issue 3, 2006, Pages 390-404

  Heydecke, Diana ^a   Meyer, Dorke ^a   Ackermann, Frauke ^a   Wilhelm, Beate ^a   Gudermann, Thomas ^a   Boekhoff, Ingrid ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Acrosome reaction; MPDZ; Signal transduction

Indexed keywords

MEMBRANE PROTEIN; PDZ PROTEIN; PROTEIN ANTIBODY; PROTEIN INAD; PROTEIN MUPP1; UNCLASSIFIED DRUG;

ACROSOME; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FERTILIZATION; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPERMATOZOON; TESTIS;

ACROSOME; ANIMALS; CARRIER PROTEINS; CATTLE; CELLS, CULTURED; HUMANS; MALE; MICE; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPERM CAPACITATION;

EID: 33646367186     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.05166     Document Type: Article

References (83)

1. Abou-Haila A, Tulsiani DR. Mammalian sperm acrosome: formation, contents, and function. Arch Biochem Biophys. 2000;379:173-182.
2. Aigner A, Ray PE, Czubayko F, Wellstein A. Immunolocalization of an FGF-binding protein reveals a widespread expression pattern during different stages of mouse embryo development. Histochem Cell Biol. 2002;117:1-11.
3. Arnoult C, Cardullo RA, Lemos JR, Florman HM. Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci U S A. 1996;93:13004-13009.
4. Austin CR. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res (B). 1951;4:581-596.
5. Aviles M, Castells MT, Martinez-Menarguez JA, Abascal I, Ballesta J. Localization of penultimate carbohydrate residues in zona pellucida and acrosomes by means of lectin cytochemistry and enzymatic treatments. Histochem J. 1997;29:583-592.
6. Barritt DS, Pearn MT, Zisch AH, Lee SS, Javier RT, Pasquale EB, Stallcup WB. The multi-PDZ domain protein MUPP1 is a cytoplasmic ligand for the membrane-spanning proteoglycan NG2. J Cell Biochem. 2000;79:213-224.
7. Bearer EL, Friend DS. Morphology of mammalian sperm membranes during differentiation, maturation, and capacitation. J Electron Microsc Tech. 1990;16:281-297.
8. Becamel C, Figge A, Poliak S, Dumuis A, Peles E, Bockaert J, Lubbert H, Ullmer C. Interaction of serotonin 5-hydroxytryptamine type 2C receptors with PDZ10 of the multi-PDZ domain protein MUPP1. J Biol Chem. 2001;276:12974-12982.
9. Bleil JD, Wassarman PM. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol. 1983;95:317-324.
10. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
11. Breitbart H. Role and regulation of intracellular calcium in acrosomal exocytosis. J Reprod Immunol. 2002;53:151-159.
12. Breitbart H, Spungin B. The biochemistry of the acrosome reaction. Mol Hum Reprod. 1997;3:195-202.
13. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 1951;168:697-698.
14. Coyne CB, Voelker T, Pichla SL, Bergelson JM. The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J Biol Chem. 2004;279:48079-48084.
15. Darszon A, Beltran C, Felix R, Nishigaki T, Trevino CL. Ion transport in sperm signaling. Dev Biol. 2001;240:1-14.
16. Eddy E, O'Brien D. The spermatozoon. In: E Knobil, J Neill eds. The Physiology of Reproduction. New York, NY: Raven Press; 1994;29-77.
17. Fan JS, Zhang M. Signaling complex organization by PDZ domain proteins. Neurosignals. 2002;11:315-321.
18. Fanning AS, Anderson JM. Protein modules as organizers of membrane structure. Curr Opin Cell Bio. 1999;11:432-439.
19. Fawcett DW. The mammalian spermatozoon. Dev Biol. 1975;44:394-436.
20. Feng H, Sandlow JI, Sandra A. Expression and function of the c-kit proto-oncogene protein in mouse sperm. Biol Reprod. 1997;57:194-203.
21. Feng H, Sandlow JI, Sandra A. The c-kit receptor and its possible signaling transduction pathway in mouse spermatozoa. Mol Reprod Dev. 1998;49:317-326.
22. Feng HL, Sandlow JI, Zheng LJ. C-kit receptor and its possible function in human spermatozoa. Mol Reprod Dev. 2005;70:103-110.
23. Flesch FM, Gadella BM. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta. 2000;1469:197-235.
24. Florman HM, Arnoult C, Kazam IG, Li C, O'Toole CM. A perspective on the control of mammalian fertilization by egg-activated ion channels in sperm: a tale of two channels. Biol Reprod. 1998;59:12-16.
25. Fukami K, Yoshida M, Inoue T, Kurokawa M, Fissore RA, Yoshida N, Mikoshiba K, Takenawa T. Phospholipase Cdelta4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J Cell Biol. 2003;161:79-88.
26. Gliki G, Ebnet K, Aurrand-Lions M, Imhof BA, Adams RH. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature. 2004;431:320-324.
27. Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S. Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem. 2002;277:455-461.
28. Harris BZ, Lim WA. Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci. 2001;114:3219-3231.
29. Hofmann MC, Hess RA, Goldberg E, Millan JL. Immortalized germ cells undergo meiosis in vitro. Proc Natl Acad Sci U S A. 1994;91:5533-5537.
30. Hofmann MC, Narisawa S, Hess RA, Millan JL. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res. 1992;201:417-435.
31. Huber A. Scaffolding proteins organize multimolecular protein complexes for sensory signal transduction. Eur J Neurosci. 2001;14:769-776.
32. Hutt DM, Cardullo RA, Baltz JM, Ngsee JK. Synaptotagmin VIII is localized to the mouse sperm head and may function in acrosomal exocytosis. Biol Reprod. 2002;66:50-56.
33. Jahn R, Lang T, Sudhof TC. Membrane fusion. Cell. 2003;112:519-533.
34. Jeansonne B, Lu Q, Goodenough DA, Chen YH. Claudin-8 interacts with multi-PDZ domain protein 1 (MUPP1) and reduces paracellular conductance in epithelial cells. Cell Mol Biol (Noisy-legrand). 2003;49:13-21.
35. Jelen F, Oleksy A, Smietana K, Otlewski J. PDZ domains - common players in the cell signaling. Acta Biochim Pol. 2003;50:985-1017.
36. Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM. Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol. 2001;3:499-502.
37. Kim E, Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci. 2004;5:771-781.
38. Kimber WA, Trinkle-Mulcahy L, Cheung PC, Deak M, Marsden LJ, Kieloch A, Watt S, Javier RT, Gray A, Downes CP, Lucocq JM, Alessi DR. Evidence that the tandem-pleckstrin-homology-domain-containing protein TAPP1 interacts with Ptd(3,4)P2 and the multi-PDZ-domain-containing protein MUPP1 in vivo. Biochem J. 2002;361:525-536.
39. Krapivinsky G, Medina I, Krapivinsky L, Gapon S, Clapham DE. SynGAP-MUPP1-CaMKII synaptic complexes regulate p38 MAP kinase activity and NMDA receptor-dependent synaptic AMPA receptor potentiation. Neuron. 2004;43:563-574.
40. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
41. Lee SS, Glaunsinger B, Mantovani F, Banks L, Javier RT. Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J Virol. 2000;74:9680-9693.
42. Lopez-Gonzalez I, Olamendi-Portugal T, De la Vega-Beltran JL, Van der Walt J, Dyason K, Possani LD, Felix R, Darszon A. Scorpion toxins that block T-type Ca2+ channels in spermatogenic cells inhibit the sperm acrosome reaction. Biochem Biophys Res Commun. 2003;300:408-414.
43. Mancini A, Koch A, Stefan M, Niemann H, Tamura T. The direct association of the multiple PDZ domain containing proteins (MUPP-1) with the human c-Kit C-terminus is regulated by tyrosine kinase activity. FEBS Lett. 2000;482:54-58.
44. Massimi P, Gammoh N, Thomas M, Banks L. HPV E6 specifically targets different cellular pools of its PDZ domain-containing tumour suppressor substrates for proteasome-mediated degradation. Oncogene. 2004;23:8033-8039.
45. Mayer A. Membrane fusion in eukaryotic cells. Annu Rev Cell Dev Biol. 2002;18:289-314.
46. McLaughlin EA, Ford WC, Hull MG. Effects of cryopreservation on the human sperm acrosome and its response to A23187. J Reprod Fertil. 1993;99:71-76.
47. Mendoza C, Carreras A, Moos J, Tesarik J. Distinction between true acrosome reaction and degenerative acrosome loss by a one-step staining method using Pisum sativum agglutinin. J Reprod Fertil. 1992;95:755-763.
48. Michaut M, De Blas G, Tomes CN, Yunes R, Fukuda M, Mayorga LS. Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev Biol. 2001;235:521-529.
49. Michaut M, Tomes CN, De Blas G, Yunes R, Mayorga LS. Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor. Proc Natl Acad Sci U S A. 2000;97:9996-10001.
50. Montell C. Visual transduction in Drosophila. Annu Rev Cell Dev Biol. 1999;15:231-268.
51. Montell C. Molecular genetics of Drosophila TRP channels. Novartis Found Symp. 2004;258:3-12; discussion 12-17, 98-102, 263-266.
52. Naz RK, Rajesh PB. Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction. Reprod Biol Endocrinol. 2004;2:75.
53. O'Toole CM, Arnoult C, Darszon A, Steinhardt RA, Florman HM. Ca(2+) entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell. 2000;11:1571-1584.
54. Parker LL, Backstrom JR, Sanders-Bush E, Shieh BH. Agonist-induced phosphorylation of the serotonin 5-HT2C receptor regulates its interaction with multiple PDZ protein 1. J Biol Chem. 2003;278:21576-21583.
55. Pawson T, Scott JD. Signaling through scaffold, anchoring, and adaptor proteins. Science. 1997;278:2075-2080.
56. Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, Kambampati V, Mains RE, Eipper BA. The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron. 2001;29:229-242.
57. Philipp S, Flockerzi V. Molecular characterization of a novel human PDZ domain protein with homology to INAD from Drosophila melanogaster. FEBS Lett. 1997;413:243-248.
58. Prasanth SG, Chattopadhyay M, Bhat KV, Ali S. Expression of protooncogene c-kit receptor in rat testis and uniqueness of extracellular domain across the species with potential in molecular phylogeny. DNA Cell Biol. 2004;23:35-43.
59. Primakoff P, Myles DG. Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science. 2002;296:2183-2185.
60. Ramalho-Santos J, Schatten G, Moreno RD. Control of membrane fusion during spermiogenesis and the acrosome reaction. Biol Reprod. 2002;67:1043-1051.
61. Rossi P, Dolci S, Sette C, Geremia R. Molecular mechanisms utilized by alternative c-kit gene products in the control of spermatogonial proliferation and sperm-mediated egg activation. Andrologia. 2003;35:71-78.
62. Sandlow JI, Feng HL, Cohen MB, Sandra A. Expression of c-KIT and its ligand, stem cell factor, in normal and subfertile human testicular tissue. J Androl. 1996;17:403-408.
63. Sandlow JI, Feng HL, Sandra A. Localization and expression of the c-kit receptor protein in human and rodent testis and sperm. Urology. 1997;49:494-500.
64. Scott K, Zuker CS. Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses. Nature. 1998;395:805-808.
65. Sitek B, Poschmann G, Schmidtke K, Ullmer C, Maskri L, Andriske M, Stichel CC, Zhu XR, Luebbert H. Expression of MUPP1 protein in mouse brain. Brain Res. 2003;970:178-187.
66. Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci. 2004;27:509-547.
67. Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM. Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol. 2004;274:426-435.
68. Tomes CN, De Blas GA, Michaut MA, Farre EV, Cherhitin O, Visconti PE, Mayorga LS. alpha-SNAP and NSF are required in a priming step during the human sperm acrosome reaction. Mol Hum Reprod. 2005;11:43-51.
69. Tomes CN, Michaut M, De Blas G, Visconti P, Matti U, Mayorga LS. SNARE complex assembly is required for human sperm acrosome reaction. Dev Biol. 2002;243:326-338.
70. Tsunoda S, Sun Y, Suzuki E, Zuker C. Independent anchoring and assembly mechanisms of INAD signaling complexes in Drosophila photoreceptors. J Neurosci. 2001;21:150-158.
71. Tulsiani DR, Abou-Haila A, Loeser CR, Pereira BM. The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp Cell Res. 1998;240:151-164.
72. Ullmer C, Schmuck K, Figge A, Lubbert H. Cloning and characterization of MUPP1, a novel PDZ domain protein. FEBS Lett. 1998;424:63-68.
73. van de Pavert SA, Kantardzhieva A, Malysheva A, Meuleman J, Versteeg I, Levelt C, Klooster J, Geiger S, Seeliger MW, Rashbass P, Le Bivic A, Wijnholds J. Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci. 2004;117:4169-4177.
74. van Ham M, Hendriks W. PDZ domains-glue and guide. Mol Biol Rep. 2003;30:69-82.
75. Ward CR, Storey BT, Kopf GS. Selective activation of Gi1 and Gi2 in mouse sperm by the zona pellucida, the egg's extracellular matrix. J Biol Chem. 1994;269:13254-13258.
76. Wassarman PM. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell. 1999;96:175-183.
77. Wassarman PM, Jovine L, Litscher ES. A profile of fertilization in mammals. Nat Cell Biol. 2001;3:E59-64.
78. Wei G, Mahowald AP. The germline: familiar and newly uncovered properties. Annu Rev Genet. 1994;28:309-324.
79. Wennemuth G, Westenbroek RE, Xu T, Hille B, Babcock DF. CaV2.2 and CaV2.3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem. 2000;275:21210-21217.
80. Yanagimachi R. Mammalian fertilization. In: E Knobil, J Neill eds. The Physiology of Reproduction. New York, NY: Raven Press; 1994;189-317.
81. Yoshinaga K, Toshimori K. Organization and modifications of sperm acrosomal molecules during spermatogenesis and epididymal maturation. Microsc Res Tech. 2003;61:39-45.
82. Yunes R, Tomes C, Michaut M, De Blas G, Rodriguez F, Regazzi R, Mayorga LS. Rab3A and calmodulin regulate acrosomal exocytosis by mechanisms that do not require a direct interaction. FEBS Lett. 2002;525:126-130.
83. Ziegler BL, Lamping C, Thoma S, Thomas CA. Single-cell cDNA-PCR: removal of contaminating genomic DNA from total RNA using immobilized DNase I. Biotechniques. 1992;13:726-729.