Fibroblast growth factor receptors (FGFRs) in human sperm: Expression, functionality and involvement in motility regulation

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Saucedo, Lucía ^a   Buffa, Gabriela N ^a   Rosso, Marina ^a   Guillardoy, Tomás ^a   Góngora, Adrian ^a   Munuce, María J ^b,c   Vazquez Levin, Mónica H ^a   Marín Briggiler, Clara ^a  

^a Instituto de Biología Y Medicina Experimental ^*  (Argentina)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^c Reprolab Sanatorio Británico de Rosario ^*  (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GERM CELL; HUMAN; HUMAN CELL; MALE; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPERMATOZOON MOTILITY; CYTOLOGY; GENE EXPRESSION; GENETICS; MCF-7 CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SEMINIFEROUS TUBULE; SPERMATOZOON;

MAMMALIA;

FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION; HUMANS; MALE; MCF-7 CELLS; PROTEIN TRANSPORT; RECEPTORS, FIBROBLAST GROWTH FACTOR; SEMINIFEROUS TUBULES; SIGNAL TRANSDUCTION; SPERM MOTILITY; SPERMATOZOA;

EID: 84929327250     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127297     Document Type: Article

References (53)

1. Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2: REVIEWS3005. PMID: 11276432
2. Yu PJ, Ferrari G, Galloway AC, Mignatti P, Pintucci G (2007) Basic fibroblast growth factor (FGF-2): the high molecular weight forms come of age. J Cell Biochem 100: 1100-1108. PMID: 17131363
3. Givol D, Yayon A (1992) Complexity of FGF receptors: genetic basis for structural diversity and functional specificity. FASEB J 6: 3362-3369. PMID: 1464370
4. Johnson DE, Williams LT (1993) Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60: 1-41. PMID: 8417497
5. Powers CJ, McLeskey SW, Wellstein A (2000) Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7: 165-197. PMID: 11021964
6. Cotton LM, O'Bryan MK, Hinton BT (2008) Cellular signaling by fibroblast growth factors (FGFs) and their receptors (FGFRs) in male reproduction. Endocr Rev 29: 193-216. doi: 10.1210/er.2007-0028 PMID: 18216218
7. Mohammadi M, Olsen SK, Ibrahimi OA (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev 16: 107-137. PMID: 15863029
8. Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149. PMID: 15863030
9. Hughes SE (1997) Differential expression of the fibroblast growth factor receptor (FGFR) multigene family in normal human adult tissues. J Histochem Cytochem 45: 1005-1019. PMID: 9212826
10. Fon Tacer K, Bookout AL, Ding X, Kurosu H, John GB, Wang L, et al. (2010) Research resource: Comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 24: 2050-2064. doi: 10.1210/me.2010-0142 PMID: 20667984
11. Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10: 116-129. doi: 10.1038/nrc2780 PMID: 20094046
12. Itoh N, Ornitz DM (2011) Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem 149: 121-130. doi: 10.1093/jb/mvq121 PMID: 20940169
13. Dorey K, Amaya E (2010) FGF signalling: diverse roles during early vertebrate embryogenesis. Development 137: 3731-3742. doi: 10.1242/dev.037689 PMID: 20978071
14. Chaves RN, de Matos MH, Buratini J Jr, de Figueiredo JR (2012) The fibroblast growth factor family: involvement in the regulation of folliculogenesis. Reprod Fertil Dev 24: 905-915. doi: 10.1071/RD11318 PMID: 22935151
15. Jiang X, Skibba M, Zhang C, Tan Y, Xin Y, Qu Y (2013) The roles of fibroblast growth factors in the testicular development and tumor. J Diabetes Res 2013: 489095. doi: 10.1155/2013/489095 PMID: 24159602
16. Xu B, Yang L, Hinton BT (2013) The role of fibroblast growth factor receptor substrate 2 (FRS2) in the regulation of two activity levels of the components of the extracellular signal-regulated kinase (ERK) pathway in the mouse epididymis. Biol Reprod 89: 1-13.
17. Cotton L, Gibbs GM, Sanchez-Partida LG, Morrison JR, de Kretser DM, O'Bryan MK (2006) FGFR-1 [corrected] signaling is involved in spermiogenesis and sperm capacitation. J Cell Sci 119: 75-84. PMID: 16352663
18. Li S, Lan ZJ, Li X, Lin J, Lei Z (2014) Role of postnatal expression of fgfr1 and fgfr2 in testicular germ cells on spermatogenesis and fertility in mice. J Reprod Infertil 15: 122-33. PMID: 25202669
19. Giulianelli S, Cerliani JP, Lamb CA, Fabris VT, Bottino MC, Gorostiaga MA, et al. (2008) Carcinoma-associated fibroblasts activate progesterone receptors and induce hormone independent mammary tumor growth: A role for the FGF-2/FGFR-2 axis. Int J Cancer 123: 2518-2531. doi: 10.1002/ijc.23802 PMID: 18767044
20. Guagnano V, Furet P, Spanka C, Bordas V, Le Douget M, Stamm C, et al. (2011) Discovery of 3-(2,6-dichloro-3,5-dimethoxy-phenyl)-1-{6-[4-(4-ethyl-piperazin-1-yl)-phenylamino]-pyrimidin-4-yl}-1-methylurea (NVPBGJ398), a potent and selective inhibitor of the fibroblast growth factor receptor family of receptor tyrosine kinase. J Med Chem 54: 7066-7083. doi: 10.1021/jm2006222 PMID: 21936542
21. World Health Organization (2010) WHO Laboratory manual for the examination and processing of human semen, 5th edn. World Health Organization Press, Geneva, Switzerland.
22. Lehtola L, Partanen J, Sistonen L, Korhonen J, Wärri A, Härkönen P, et al. (1992) Analysis of tyrosine kinase mRNAs including four FGF receptor mRNAs expressed in MCF-7 breast-cancer cells. Int J Cancer 50: 598-603. PMID: 1311287
23. Lapyckyj L, Castillo LF, Matos ML, Gabrielli NM, Lüthy IA, Vazquez-Levin MH (2010) Expression analysis of epithelial cadherin and related proteins in IBH-6 and IBH-4 human breast cancer cell lines. J Cell Physiol 222: 596-605. doi: 10.1002/jcp.21974 PMID: 19957299
24. Marín-Briggiler CI, Veiga MF, Matos ML, Echeverría MF, Furlong LI, Vazquez-Levin MH (2008) Expression of epithelial cadherin in the human male reproductive tract and gametes and evidence of its participation in fertilization. Mol Hum Reprod 14: 561-571. doi: 10.1093/molehr/gan053 PMID: 18829448
25. Widberg CH, Newell FS, Bachmann AW, Ramnoruth SN, Spelta MC, Whitehead JP, et al. (2009) Fibroblast growth factor receptor 1 is a key regulator of early adipogenic events in human preadipocytes. Am J Physiol Endocrinol Metab 296: 121-131.
26. Marín-Briggiler CI, Lapyckyj L, González Echeverría MF, Rawe VY, Alvarez Sedó C, Vazquez-Levin MH (2010) Neural cadherin is expressed in human gametes and participates in sperm-oocyte interaction events. Int J Androl 33: e228-239. doi: 10.1111/j.1365-2605.2009.00999.x PMID: 19840148
27. Almog T, Lazar S, Reiss N, Etkovitz N, Milch E, Rahamim N, et al. (2008) Identification of extracellular signal-regulated kinase 1/2 and p38 MAPK as regulators of human sperm motility and acrosome reaction and as predictors of poor spermatozoan quality. J Biol Chem 283: 14479-14489. doi: 10.1074/jbc.M710492200 PMID: 18372245
28. Cancilla B, Davies A, Ford-Perriss M, Risbridger GP (2000) Discrete cell- and stage-specific localisation of fibroblast growth factors and receptor expression during testis development. J Endocrinol 164: 149-159. PMID: 10657850
29. Ewen KA, Olesen IA, Winge SB, Nielsen AR, Nielsen JE, Graem N, et al. (2013) Expression of FGFR3 during human testis development and in germ cell-derived tumours of young adults. Int J Dev Biol 57: 141-151. doi: 10.1387/ijdb.130022er PMID: 23784824
30. Steger K, Tetens F, Seitz J, Grothe C, Bergmann M (1998) Localization of fibroblast growth factor 2 (FGF-2) protein and the receptors FGFR 1-4 in normal human seminiferous epithelium. Histochem Cell Biol 110: 57-62. PMID: 9681690
31. von Kopylow K, Staege H, Schulze W, Will H, Kirchhoff C (2012) Fibroblast growth factor receptor 3 is highly expressed in rarely dividing human type A spermatogonia. Histochem Cell Biol 138: 759-772. doi: 10.1007/s00418-012-0991-7 PMID: 22777346
32. Maher PA (1996) Nuclear Translocation of fibroblast growth factor (FGF) receptors in response to FGF-2. J Cell Biol 134: 529-536. PMID: 8707835
33. Schmahl J, Kim Y, Colvin JS, Ornitz DM, Capel B (2004) Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 131: 3627-3636. PMID: 15229180
34. Cerliani JP, Guillardoy T, Giulianelli S, Vaque JP, Gutkind JS, Vanzulli SI, et al. (2011) Interaction between FGFR-2, STAT5, and progesterone receptors in breast cancer. Cancer Res 71: 3720-3731. doi: 10.1158/0008-5472.CAN-10-3074 PMID: 21464042
35. Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, et al. (1990) Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 9: 2685-2692. PMID: 1697263
36. Groth C, Lardelli M (2002) The structure and function of vertebrate fibroblast growth factor receptor 1. Int J Dev Biol 46: 393-400. PMID: 12141425
37. St Bernard R, Zheng L, Liu W, Winer D, Asa SL, Ezzat S (2005) Fibroblast growth factor receptors as molecular targets in thyroid carcinoma. Endocrinology 146: 1145-1153. PMID: 15564323
38. Yan D, Chen D, Cool SM, van Wijnen AJ, Mikecz K, Murphy G, et al. (2011) Fibroblast growth factor receptor 1 is principally responsible for fibroblast growth factor 2-induced catabolic activities in human articular chondrocytes. Arthritis Res Ther 13: R130. doi: 10.1186/ar3441 PMID: 21835001
39. Bellot F, Crumley G, Kaplow JM, Schlessinger J, Jaye M, Dionne CA (1991) Ligand-induced transphosphorylation between different FGF receptors. EMBO J 10: 2849-2854. PMID: 1655404
40. Bae JH, Schlessinger J (2010) Asymmetric tyrosine kinase arrangements in activation or autophosphorylation of receptor tyrosine kinases. Mol Cells 29: 443-448. doi: 10.1007/s10059-010-0080-5 PMID: 20432069
41. Luconi M, Barni T, Vannelli GB, Krausz C, Marra F, Benedetti PA, et al. (1998) Extracellular signal-regulated kinases modulate capacitation of human spermatozoa. Biol Reprod 58: 1476-1489. PMID: 9623609
42. Luconi M, Marra F, Gandini L, Filimberti E, Lenzi A, Forti G, et al. (2001) Phosphatidylinositol 3-kinase inhibition enhances human sperm motility. Hum Reprod 16: 1931-1937. PMID: 11527900
43. de Lamirande E, Gagnon C (2002) The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod 8: 124-135. PMID: 11818515
44. Koppers AJ, Mitchell LA, Wang P, Lin M, Aitken RJ (2011) Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochem J 436: 687-698. doi: 10.1042/BJ20110114 PMID: 21470189
45. Sagare-Patil V, Galvankar M, Satiya M, Bhandari B, Gupta SK, Modi D (2012) Differential concentration and time dependent effects of progesterone on kinase activity, hyperactivation and acrosome reaction in human spermatozoa. Int J Androl 35: 633-644. doi: 10.1111/j.1365-2605.2012.01291.x PMID: 22775762
46. Sugihara K, Shibata TK, Takata K, Kimura T, Kanayama N, Williams R, et al. (2013) Attenuation of fibroblast growth factor signaling by poly-N-acetyllactosamine type glycans. FEBS Lett 587: 3195-3201. doi: 10.1016/j.febslet.2013.07.056 PMID: 23968720
47. Tardif S, Madamidola OA, Brown SG, Frame L, Lefièvre L, Wyatt PG, et al. (2014) Clinically relevant enhancement of human sperm motility using compounds with reported phosphodiesterase inhibitor activity. Hum Reprod 29: 2123-2135. doi: 10.1093/humrep/deu196 PMID: 25124668
48. Pintucci G, Moscatelli D, Saponara F, Biernacki PR, Baumann FG, Bizekis C, et al. (2002) Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. FASEB J. 16: 598-600. PMID: 11919166
49. Kamura S, Matsumoto Y, Fukushi JI, Fujiwara T, Iida K, Okada Y, et al. (2010) Basic fibroblast growth factor in the bone microenvironment enhances cell motility and invasion of Ewing's sarcoma family of tumours by activating the FGFR1-PI3K-Rac1 pathway. Br J Cancer 103: 370-381. doi: 10.1038/sj.bjc.6605775 PMID: 20606682
50. Gabler C, Lauer B, Einspanier A, Schams D, Einspanier R (1997) Detection of mRNA and immunoreactive proteins for acidic and basic fibroblast growth factor and expression of the fibroblast growth factor receptors in the bovine oviduct. J Reprod Fertil 109: 213-221. PMID: 9155730
51. Malamitsi-Puchner A, Sarandakou A, Baka SG, Tziotis J, Rizos D, Hassiakos D, et al. (2001) Concentrations of angiogenic factors in follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity and fertilization. Fertil Steril 76: 98-101. PMID: 11438326
52. de Lamirande E, O'Flaherty C (2008) Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta 1784: 106-115. PMID: 17920343
53. Breitbart H, Rotman T, Rubinstein S, Etkovitz N (2010) Role and regulation of PI3K in sperm capacitation and the acrosome reaction. Mol Cell Endocrinol 314: 234-238. doi: 10.1016/j.mce.2009.06.009 PMID: 19560510