TMEM203 is a novel regulator of intracellular calcium homeostasis and is required for spermatogenesis

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Shambharkar, Prashant B ^a,b   Bittinger, Mark ^a   Latario, Brian ^a   Xiong, ZhaoHui ^a   Bandyopadhyay, Somnath ^a   Davis, Vanessa ^a   Lin, Victor ^a   Yang, Yi ^a   Valdez, Reginald ^a   Labow, Mark A ^a  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b Celgene Avilomics Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; COMPLEMENTARY DNA; MEMBRANE PROTEIN; TRANSMEMBRANE 203 PROTEIN; UNCLASSIFIED DRUG; CALCINEURIN; PROTEIN BINDING; TMEM203 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPERMATOCYTE; SPERMATOGENESIS; TESTIS; ANIMAL; CALCIUM SIGNALING; CELL LINE; EPIDIDYMIS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; INTRACELLULAR SPACE; KNOCKOUT MOUSE; MALE INFERTILITY; METABOLISM; PATHOLOGY;

MUS;

ANIMALS; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CELL LINE; ENDOPLASMIC RETICULUM; EPIDIDYMIS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INFERTILITY, MALE; INTRACELLULAR SPACE; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN BINDING; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 84930677032     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127480     Document Type: Article

References (54)

1. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21. PMID: 11413485
2. Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32: 235-249. PMID: 12543086
3. Carafoli E (2002) Calcium signaling: a tale for all seasons. Proc Natl Acad Sci U S A 99: 1115-1122. PMID: 11830654
4. Clapham DE (2007) Calcium signaling. Cell 131: 1047-1058. PMID: 18083096
5. Berridge MJ (1997) Elementary and global aspects of calcium signalling. J Physiol 499 (Pt 2): 291-306.
6. Screaton RA, Conkright MD, Katoh Y, Best JL, Canettieri G, Jeffries S et al. (2004) The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119: 61-74. PMID: 15454081
7. Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12: 141-151. doi: 10.1038/nrm3072 PMID: 21346730
8. Bittinger MA, McWhinnie E, Meltzer J, Iourgenko V, Latario B, Liu X et al. (2004) Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins. Curr Biol 14: 2156-2161. PMID: 15589160
9. Macian F (2005) NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5: 472-484. PMID: 15928679
10. Cahalan MD (2009) STIMulating store-operated Ca(2+) entry. Nat Cell Biol 11: 669-677. doi: 10.1038/ncb0609-669 PMID: 19488056
11. Hewavitharana T, Deng X, Soboloff J, Gill DL (2007) Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 42: 173-182. PMID: 17602740
12. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28: 491-533. doi: 10.1146/annurev.immunol.021908.132550 PMID: 20307213
13. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85: 757-810. PMID: 15788710
14. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, et al. (2003) Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162: 59-69. PMID: 12847083
15. Rong Y, Distelhorst CW (2008) Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70: 73-91. PMID: 17680735
16. Berridge MJ (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 1793: 933-940. doi: 10.1016/j.bbamcr.2008.10.005 PMID: 19010359
17. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, et al. (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413: 603-609. PMID: 11595941
18. Darszon A, Nishigaki T, Beltran C, Trevino CL (2011) Calcium channels in the development, maturation, and function of spermatozoa. Physiol Rev 91: 1305-1355. doi: 10.1152/physrev.00028.2010 PMID: 22013213
19. Navarro B, Kirichok Y, Chung JJ, Clapham DE (2008) Ion channels that control fertility in mammalian spermatozoa. Int J Dev Biol 52: 607-613. doi: 10.1387/ijdb.072554bn PMID: 18649274
20. Wakai T, Vanderheyden V, Fissore RA. (2011) Ca2+ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harb Perspect Biol 3.
21. Tosti E (2006) Calcium ion currents mediating oocyte maturation events. Reprod Biol Endocrinol 4: 26. PMID: 16684344
22. Gorczynska-Fjalling E (2004) The role of calcium in signal transduction processes in Sertoli cells. Reprod Biol 4: 219-241. PMID: 15592583
23. Cheng CY, Mruk DD (2010) The biology of spermatogenesis: the past, present and future. Philos Trans R Soc Lond B Biol Sci 365: 1459-1463. doi: 10.1098/rstb.2010.0024 PMID: 20403863
24. Cooke HJ, Saunders PT (2002) Mouse models of male infertility. Nat Rev Genet 3: 790-801. PMID: 12360237
25. Mruk DD, Cheng CY (2004) Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25: 747-806. PMID: 15466940
26. Maclean JA, Wilkinson MF (2005) Gene regulation in spermatogenesis. Curr Top Dev Biol 71: 131-197. PMID: 16344105
27. Naz RK, Engle A, None R (2009) Gene knockouts that affect male fertility: novel targets for contraception. Front Biosci (Landmark Ed) 14: 3994-4007. PMID: 19273329
28. Latendresse JR, Warbrittion AR, Jonassen H, Creasy DM (2002) Fixation of testes and eyes using a modified Davidson's fluid: comparison with Bouin's fluid and conventional Davidson's fluid. Toxicol Pathol 30: 524-533. PMID: 12187944
29. OAKBERG EF (1956) A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 99: 391-413. PMID: 13402725
30. OAKBERG EF (1956) Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99: 507-516. PMID: 13402729
31. Russell LB (1990) Patterns of mutational sensitivity to chemicals in poststem-cell stages of mouse spermatogenesis. Prog Clin Biol Res 340C: 101-113. PMID: 2199974
32. Kauffmann A, Gentleman R, Huber W (2009) arrayQualityMetrics - a bioconductor package for quality assessment of microarray data. Bioinformatics 25: 415-416. doi: 10.1093/bioinformatics/btn647 PMID: 19106121
33. Katz S, Irizarry RA, Lin X, Tripputi M, Porter MW (2006) A summarization approach for Affymetrix Gene- Chip data using a reference training set from a large, biologically diverse database. BMC Bioinformatics 7: 464. PMID: 17059591
34. Wettenhall JM, Smyth GK (2004) limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706. PMID: 15297296
35. Bailey S, Macardle PJ (2006) A flow cytometric comparison of Indo-1 to fluo-3 and Fura Red excited with low power lasers for detecting Ca(2+) flux. J Immunol Methods 311: 220-225. PMID: 16545393
36. Ohta H, Sakaide Y, Wakayama T (2007) Generation of progeny via ICSI following enrichment of elongated spermatids from mouse testis by flow-cytometric cell sorting. Hum Reprod 22: 1612-1616. PMID: 17428882
37. Coultas L, Bouillet P, Loveland KL, Meachem S, Perlman H, Adams JM, et al. (2005) Concomitant loss of proapoptotic BH3-only Bcl-2 antagonists Bik and Bim arrests spermatogenesis. EMBO J 24: 3963-3973. PMID: 16270031
38. Jousset H, Frieden M, Demaurex N (2007) STIM1 knockdown reveals that store-operated Ca2+ channels located close to sarco/endoplasmic Ca2+ ATPases (SERCA) pumps silently refill the endoplasmic reticulum. J Biol Chem 282: 11456-11464. PMID: 17283081
39. Manjarres IM, Rodriguez-Garcia A, Alonso MT, Garcia-Sancho J (2010) The sarco/endoplasmic reticulum Ca(2+) ATPase (SERCA) is the third element in capacitative calcium entry. Cell Calcium 47: 412-418. doi: 10.1016/j.ceca.2010.03.001 PMID: 20347143
40. Lopez JJ, Jardin I, Bobe R, Pariente JA, Enouf J, Salido GM, et al. (2008) STIM1 regulates acidic Ca2+ store refilling by interaction with SERCA3 in human platelets. Biochem Pharmacol 75: 2157-2164. doi: 10.1016/j.bcp.2008.03.010 PMID: 18439569
41. Waser M, Mesaeli N, Spencer C, Michalak M (1997) Regulation of calreticulin gene expression by calcium. J Cell Biol 138: 547-557. PMID: 9245785
42. Matsuo K, Galson DL, Zhao C, Peng L, Laplace C, Wang KZ, et al. (2004) Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J Biol Chem 279: 26475-26480. PMID: 15073183
43. Tu H, Nelson O, Bezprozvanny A, Wang Z, Lee SF, Hao YH, et al. (2006) Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 126: 981-993. PMID: 16959576
44. Bultynck G, Kiviluoto S, Henke N, Ivanova H, Schneider L, Rybalchenko V, et al. (2012) The C terminus of Bax inhibitor-1 forms a Ca2+-permeable channel pore. J Biol Chem 287: 2544-2557. doi: 10.1074/jbc.M111.275354 PMID: 22128171
45. Szegezdi E, Macdonald DC, Ni CT, Gupta S, Samali A (2009) Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol 296: C941-C953. doi: 10.1152/ajpcell.00612.2008 PMID: 19279228
46. Pan Z, Bhat MB, Nieminen AL, Ma J (2001) Synergistic movements of Ca(2+) and Bax in cells undergoing apoptosis. J Biol Chem 276: 32257-32263. PMID: 11413128
47. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, et al. (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300: 135-139. PMID: 12624178
48. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, Pozzan T, et al. (2005) Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci U S A 102: 105-110. PMID: 15613488
49. Ferdek PE, Gerasimenko JV, Peng S, Tepikin AV, Petersen OH, Gerasimenko OV (2012) A novel role for Bcl-2 in regulation of cellular calcium extrusion. Curr Biol 22: 1241-1246. doi: 10.1016/j.cub.2012.05.002 PMID: 22704985
50. Bandyopadhyay J, Lee J, Lee J, Lee JI, Yu JR, Jee C, et al. (2002) Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol Biol Cell 13: 3281-3293. PMID: 12221132
51. Park BJ, Lee DG, Yu JR, Jung SK, Choi K, Lee J, et al. (2001) Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell 12: 2835-2845. PMID: 11553721
52. Yuan W, Leisner TM, McFadden AW, Clark S, Hiller S, Maeda N, et al. (2006) CIB1 is essential for mouse spermatogenesis. Mol Cell Biol 26: 8507-8514. PMID: 16982698
53. White C, Yang J, Monteiro MJ, Foskett JK (2006) CIB1, a ubiquitously expressed Ca2+-binding protein ligand of the InsP3 receptor Ca2+ release channel. J Biol Chem 281: 20825-20833. PMID: 16723353
54. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99. PMID: 7569956