Phosphatidylinositol 4-phosphate 5-kinase is indispensable for mouse spermatogenesis

Biology of Reproduction

Volumn 86, Issue 5, 2012, Pages

  Hasegawa, Hiroshi ^a   Noguchi, Junko ^b   Yamashita, Misuzu ^a   Okada, Risa ^a   Sugimoto, Rika ^a   Furuya, Momoko ^a   Unoki, Takamitsu ^a   Funakoshi, Yuji ^a   Baba, Tadashi ^a   Kanaho, Yasunori ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Development; Fertility; Knockout mouse; Phosphatidylinositol 4 phosphate 5 kinase; Spermatogenesis; Testis

Indexed keywords

F ACTIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; 1-PHOSPHATIDYLINOSITOL-4-PHOSPHATE 5-KINASE; ACTIN; ISOENZYME; PHOSPHOTRANSFERASE;

ARTICLE; CELL MEMBRANE; FERTILITY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SPERM; SPERMATID; SPERMATOGENESIS; ANIMAL; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; SPERMATOZOON TAIL;

MAMMALIA; MUS;

ACTINS; ANIMALS; ISOENZYMES; MALE; MICE; MICE, KNOCKOUT; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); SEMINIFEROUS EPITHELIUM; SEMINIFEROUS TUBULES; SPERM TAIL; SPERMATIDS; SPERMATOGENESIS;

EID: 84863992782     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.089896     Document Type: Article

References (48)

1. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 1999; 99: 521-532.
2. Sechi AS, Wehland J. The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J Cell Sci 2000; 113:3685-3695.
3. Takenawa T, Itoh T, Fukami K. Regulation of phosphatidylinositol 4,5-bisphosphate levels and its roles in cytoskeletal re-organization and malignant transformation. Chem Phys Lipids 1999; 98:13-22.
4. Yin HL, Janmey PA. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 2003; 65:761-789.
5. Downes CP, Gray A, Lucocq JM. Probing phosphoinositide functions in signaling and membrane trafficking. Trends Cell Biol 2005; 15:259-268.
6. Martin TF. PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol 2001; 13:493-499.
7. Hilgemann DW, Feng S, Nasuhoglu C. The complex and intriguing lives of PIP2 with ion channels and transporters. Sci STKE 2001; 2001; RE19.
8. Ma HP, Saxena S, Warnock DG. Anionic phospholipids regulate native and expressed epithelial sodium channel (ENaC). J Biol Chem 2002; 277: 7641-7644.
9. Prescott ED, Julius D. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 2003; 300:1284-1288.
10. Martin-Belmonte F, Mostov K. Phosphoinositides control epithelial development. Cell Cycle 2007; 6:1957-1961.
11. Bunce MW, Bergendahl K, Anderson RA. Nuclear PI(4,5)P(2): a new place for an old signal. Biochim Biophys Acta 2006; 1761:560-569.
12. Mejillano M, Yamamoto M, Rozelle AL, Sun HQ, Wang X, Yin HL. Regulation of apoptosis by phosphatidylinositol 4,5-bisphosphate inhibition of caspases, and caspase inactivation of phosphatidylinositol phosphate 5-kinases. J Biol Chem 2001; 276:1865-1872.
13. Ishihara H, Shibasaki Y, Kizuki N, Katagiri H, Yazaki Y, Asano T, Oka Y. Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J Biol Chem 1996; 271: 23611-23614.
14. Ishihara H, Shibasaki Y, Kizuki N, Wada T, Yazaki Y, Asano T, Oka Y. Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J Biol Chem 1998; 273:8741-8748.
15. Loijens JC, Anderson RA. Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J Biol Chem 1996; 271:32937-32943.
16. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, Voronov S, Chang S, Guo J, Wenk MR, De Camilli P. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 2002; 420:85-89.
17. Gonzales ML, Anderson RA. Nuclear phosphoinositide kinases and inositol phospholipids. J Cell Biochem 2006; 97:252-260.
18. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 2002; 420:89-93.
19. Nakano-Kobayashi A, Yamazaki M, Unoki T, Hongu T, Murata C, Taguchi R, Katada T, Frohman MA, Yokozeki T, Kanaho Y. Role of activation of PIP5Kgamma661 by AP-2 complex in synaptic vesicle endocytosis. EMBO J 2007; 26:1105-1116.
20. Weernink PA, Meletiadis K, Hommeltenberg S, Hinz M, Ishihara H, Schmidt M, Jakobs KH. Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J Biol Chem 2004; 279:7840-7849.
21. Di Paolo G, Moskowitz HS, Gipson K, Wenk MR, Voronov S, Obayashi M, Flavell R, Fitzsimonds RM, Ryan TA, De Camilli P. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 2004; 431:415-422.
22. Sasaki J, Sasaki T, Yamazaki M, Matsuoka K, Taya C, Shitara H, Takasuga S, Nishio M, Mizuno K, Wada T, Miyazaki H, Watanabe H, et al. Regulation of anaphylactic responses by phosphatidylinositol phosphate kinase type I falphag. J Exp Med 2005; 201:859-870.
23. Wang Y, Lian L, Golden JA, Morrisey EE, Abrams CS. PIP5KI gamma is required for cardiovascular and neuronal development. Proc Natl Acad Sci U S A 2007; 104:11748-11753.
24. Wang Y, Chen X, Lian L, Tang T, Stalker TJ, Sasaki T, Kanaho Y, Brass LF, Choi JK, Hartwig JH, Abrams CS. Loss of PIP5KIbeta demonstrates that PIP5KI isoform-specific PIP2 synthesis is required for IP3 formation. Proc Natl Acad Sci U S A 2008; 105:14064-14069.
25. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747-806.
26. Yan HH, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or a foe of spermatogenesis? Bioessays 2007; 29:36-48.
27. Siu MK, Mruk DD, Lee WM, Cheng CY. Adhering junction dynamics in the testis are regulated by an interplay of beta 1-integrin and focal adhesion complex-associated proteins. Endocrinology 2003; 144: 2141-2163.
28. Siu MK, Wong CH, Lee WM, Cheng CY. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 2005; 280:25029-25047.
29. Johnson L, and Neaves, WB. Enhanced daily production in the remaining testis of aged rats following hemicastration. J Androl 1983; 4:162-166.
30. Toyoda M, Yokoyama M, Hoshi T. Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn J Anim Reprod 1971; 16:147-151.
31. Tanii I, Araki S, Toshimori K. Intra-acrosomal organization of a 90-kilodalton antigen during spermiogenesis in the rat. Cell Tissue Res 1994; 277:61-67.
32. 125I-BMIPP autoradiography. Ann Nucl Med 2004; 18:195-202.
33. Yamashita M, Honda A, Ogura A, Kashiwabara S, Fukami K, Baba T. Reduced fertility of mouse epididymal sperm lacking Prss21/Tesp5 is rescued by sperm exposure to uterine microenvironment. Genes Cells 2008; 13:1001-1013.
34. Don J, Winer MA, Wolgemuth DJ. Developmentally regulated expression during gametogenesis of the murine gene meg1 suggests a role in meiosis. Mol Reprod Dev 1994; 38:16-23.
35. Wu JY, Means AR. Ca2{thorn}/calmodulin-dependent protein kinase IV is expressed in spermatids and targeted to chromatin and the nuclear matrix. J Biol Chem 2000; 275:7994-7999.
36. Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 1956; 99: 507-516.
37. Ohta H, Tohda A, Nishimune Y. Proliferation and differentiation of spermatogonial stem cells in the w/wv mutant mouse testis. Biol Reprod 2003; 69:1815-1821.
38. Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999; 20:198-213.
39. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, Mueller S, Irie K, Ikeda W, Sakai T, Wimmer E, Nishimune Y, Takai Y. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 2002; 12:1145-1150.
40. Tarnasky H, Cheng M, Ou Y, Thundathil JC, Oko R, van der Hoorn FA. Gene trap mutation of murine outer dense fiber protein-2 gene can result in sperm tail abnormalities in mice with high percentage chimaerism. BMC Dev Biol 2010; 10:67.
41. Yan W. Male infertility caused by spermiogenic defects: lessons from gene knockouts. Mol Cell Endocrinol 2009; 306:24-32.
42. Wei HC, Rollins J, Fabian L, Hayes M, Polevoy G, Bazinet C, Brill JA. Depletion of plasma membrane PtdIns(4,5)P2 reveals essential roles for phosphoinositides in flagellar biogenesis. J Cell Sci 2008; 121:1076-1084.
43. Wong EW, Mruk DD, Lee WM, Cheng CY. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci U S A 2008; 105:9657-9662.
44. Guttman JA, Janmey P, Vogl AW. Gelsolin-evidence for a role in turnover of junction-related actin filaments in Sertoli cells. J Cell Sci 2002; 115:499-505.
45. Yoneda A, Kashima M, Yoshida S, Terada K, Nakagawa S, Sakamoto A, Hayakawa K, Suzuki K, Ueda J, Watanabe T. Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase Czeta. Reproduction 2006; 132:393-401.
46. Young JS, Guttman JA, Vaid KS, Shahinian H, Vogl AW. Cortactin (CTTN), N-WASP (WASL), and clathrin (CLTC) are present at podosome-like tubulobulbar complexes in the rat testis. Biol Reprod 2009; 80:153-161.
47. Kierszenbaum AL, Rivkin E, Tres LL. Acroplaxome, an F-actin-keratincontaining plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol Biol Cell 2003; 14:4628-4640.
48. Kierszenbaum AL, Tres LL. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 2004; 67:271-284.