Reproduction and human fertility: Biomedical aspects of the lipocalin family. Biology, pathobiology and bioclínica
Reproducción y fertilidad humana: Aspectos biomédicos de la familia de las lipocalinas. Biología, patobiología y bioclínica
Show authors biography
The family of lipocalin genes (LCN) is composed of several members that share a common structure and that have duplicated repeatedly during evolution, expanding to more than 150 known genes, of which at least twenty were reported in the human species. The group of proteins of the LCN is constituted by several elements that share the common property of lipophilic ligand binding. LCNs work in a wide range of systems including chemoreception and transport in sensory taste and odor physiology, coloration, hemato-immune modulation, synthesis of prostanglandin D2, neuro-physiology, reproductive physiology and fertility, embryogenesis, proliferation and cell division, survival and cellular apoptosis. Its role in pathobiology and reproductive bioclinics and fertility is evident when we observe that several LCN have altered levels of expression in different pathophysiological events. This review summarizes findings and implications. Abbreviations: LCN, lipocalinas; Gd, glycodelins; KDa, kilodalton.
Article visits 758 | PDF visits 551
Downloads
1. Flower DR. The lipocalin protein family: a role in cell regulation. FEBS Lett 1994; 354(1): 7-11.
2. PubMed [base de datos en Internet]. Bethesda, Maryland: National Library of Medicine; 1966- [citado 15 Jul 2008]. Disponible en: http://www.ncbi.nlm.nih.gov/PubMed/
3. EMBASE [base de datos en Internet]. Holanda: Excerpta Medica-Elsevier; 1974- [citado 15 Jul 2008]. Disponible en: http://www.embase.com
4. OMIM [base de datos en Internet]. Baltimore: Johns Hopkins University; 1966- [citado 15 Jul 2008]. Disponible en: http://www.ncbi.nlm.nih.gov/entrez/dispomim
5. HUGO [base de datos en Internet]. Bethesda, Maryland: National Library of Medicine, Celera Genomics and the Sanger Center; 1989- [citado 15 Jul 2008]. Disponible en: http://www.hugo-international.org/index.html
6. García GA, Clavijo D, Mejía OR, et al. Aspectos biomédicos de la familia de las lipocalinas. Univ. Méd. 2007; 48(2): 118-28.
7. García GA, García A. Aspectos biomédicos de las inmunocalinas en la especie humana. Univ. Méd. 2008; 49(1): 77-96.
8. Flower DR. Experimentally determined lipocalin structures. Biochim Biophys Acta. 2000 Oct 18;1482(1-2):46-56.
9. Flower DR, North AC, Sansom CE. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta. 2000 Oct 18;1482(1-2):9-24.
10. Flower DR. The lipocalin protein family: structure and function. Biochem J 1996; 318:1-14..
11. Sivaprasadarao A, Boudjelal M, Findlay JB. Lipocalin structure and function. Biochem Soc Trans. 1993; 21: 619-22.
12. Hayaishi O. Molecular genetic studies on sleep-wake regulation, with special emphasis on the prostaglandin D(2) system. J Appl Physiol. 2002; 92:863-8.
13. Herlong JL, Scott TR. Positioning prostanoids of the D and J series in the immunopathogenic scheme. Immunol Lett. 2006;102:121-31.
14. Maesaka JK, Palaia T, Fishbane S et al. Contribution of Prostanglandin D2 synthase to progression of renal failure and dialysis dementia. Semin Nephrol. 2002; 22: 407-14.
15. Iwa Y, Taba Y, Miyagi M, et al. Physiology and pharmacology of the prostaglandin J2 family. Nippon Yakurigaku Zasshi. 2004;123(1): 34-40.
16. Pinzar E, Kanaoka Y, Inui T, et al. Prostaglandin D synthase gene is involved in the regulation of nonrapid eye movement sleep. Proc Nat Acad Sci USA. 2000; 97: 4903-07.
17. Sasaguri T, Miwa Y. Prostaglandin J2 family and the cardiovascular system. Curr Vasc Pharmacol. 2004; 2:103-14.
18. Tanaka T, Urade Y, Kimura H et al. Lipocalin-type prostaglandin D synthase (beta-trace) is a newly recognized type of retinoid transporter. J Biol Chem 1997; 272: 15789-95.
19. Urade Y, Hayaishi O. Prostaglandin D2 and sleep regulation. Biochim Biophys Acta. 1999; 1436: 606- 15.
20. Urade Y, Hayaishi O. Prostaglandin D synthase: structure and function. Vitam Horm. 2000; 58:89-120.
21. Urade Y, Hayaishi O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim Biophys Acta. 2000;1482: 259-71.
22. Urade Y, Eguchi N. Lipocalin-type and hematopoietic prostaglandin D synthases as a novel example of functional convergence. Prostaglandins Other Lipid Mediat. 2002; 68-69:375-82.
23. García GA, Hernández S, Mejía OR, et al. Biología y patobiología humanas del complejo de absorción y transporte epitelial MegaCUBAM. Rev Fac Med Uni- versidad Militar Nueva Granada. 2007; 15(1): 94-104.
24. Faber K, Hvidberg V, Moestrup SK, et al. Megalin is a receptor for apolipoprotein M, and kidney-specific megalin-deficiency confers urinary excretion of apolipoprotein M. Mol Endocrinol. 2006;20:212-8.
25. Flower DR. Beyond the superfamily: the lipocalin receptors. Biochim Biophys Acta. 2000;1482: 327-36.
26. Hvidberg V, Jacobsen C, Strong RK, et al. The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett. 2005; 579:773-7.
27. Wojnar P, Lechner M, Mershak P et al. Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display. J Biol Chem 2001; 276: 20206-20212.
28. Wojnar P, Lechner M, Redl B. Antisense down-regulation of lipocalin-interacting membrane receptor expression inhibits cellular internalization of lipocalin-1 in human NT2 cells. J Biol Chem. 2003; 278: 16209-15.
29. Leone MG, Haq HA, Saso L. Lipocalin type prostaglandin D-synthase: which role in male fertility?. Contraception. 2002; 65:293-5.
30. Saito S, Tsuda H, Michimata T. Prostaglandin D2 and reproduction. Am J Reprod Immunol. 2002; 47: 295-302.
31. Wilhelm D, Hiramatsu R, Mizusaki H, et al. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 2007; 282:10553-60.
32. Helliwell RJ, Keelan JA, Marvin KW, et al. Gestational age-dependent up-regulation of prostaglandin D synthase (PGDS) and production of PGDS-derived antiinflammatory prostaglandins in human placenta. J Clin Endocrinol Metab. 2006; 91:597-606.
33. Alttunen M, Kamarainen M, Koistinen H. Glycodelin: a reproduction-related lipocalin. Biochim Biophys Acta 2000;1482:149-56.
34. Kontopidis G, Holt C, Sawyer L. Invited review: betalactoglobulin: binding properties, structure, and function. J Dairy Sci. 2004;87:785-96.
35. Mandelin E, Lassus H, Seppala M et al. Glycodelin in ovarian serous carcinoma: association with differentiation and survival. Cancer Res. 2003;63: 6258-64.
36. Morris HR, Dell A, Easton RL et al. Gender-specific glycosylation of human glycodelin affects its contraceptive activity. J Biol Chem. 1996; 271: 32159-67.
37. Seppälä M, Taylor RN, Koistinen H et al. Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr Rev. 2002; 23: 401-30.
38. Song M, Ramaswamy S, Ramachandran S, et al. Angiogenic role for glycodelin in tumorigenesis. Proc Nat Acad Sci USA. 2001; 98: 9265-70.
39. Yaniv E, Borovsky Z, Mishan-Eisenberg G, et al. Placental protein 14 regulates selective B cell responses. Cell Immunol. 2003; 222:156-63.
40. Dong M, Ding G, Zhou J et al. The effect of trophoblasts on T lymphocytes: possible regulatory effector moleculesa proteomic analysis. Cell Physiol Biochem. 2008;21:463-72.
41. Rawn SM, Cross JC. The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol. 2008;24:159-81.
42. Arck P, Hansen PJ, Mulac Jericevic B, et al. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am J Reprod Immunol. 2007; 58: 268-79.
43. Fujikura T, Mukai M. Prostaglandin E2 synthase in syncytiotrophoblastic vesicles found in the placental intervillous space. Am J Obstet Gynecol. 2007;196:361.
44. Athanasas-Platsis S, Somodevilla-Torres MJ, et al. Investigation of the immunocompetent cells that bind early pregnancy factor and preliminary studies of the early pregnancy factor target molecule. Immunol Cell Biol. 2004; 82: 361-9.
45. Skornicka EL, Kiyatkina N, Weber MC, et al. Pregnancy zone protein is a carrier and modulator of placental protein-14 in T-cell growth and cytokine production. Cell Immunol. 2004; 232: 144-56.
46. González A, Varo N, Alegre E, Díaz A, et al. Immunosuppression routed via the kynurenine pathway: a biochemical and pathophysiologic approach. Adv Clin Chem. 2008; 45: 155-97.
47. Kuroki K, Maenaka K. Immune modulation of HLA- G dimer in maternal-fetal interface. Eur J Immunol. 2007; 37:1727-9.
48. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy?. Semin Immunopathol. 2007; 29: 95-113.
49. Uemura Y, Suzuki M, Liu TY, et al. Role of human non-invariant NKT lymphocytes in the maintenance of type 2 T helper environment during pregnancy. Int Immunol. 2008; 20:405-12.
50. Van den Heuvel MJ, Hatta K, Peralta CG, et al. CD56+ cells are recruited to the uterus in two waves: at ovulation and during the first 2 weeks after missed menses. Am J Reprod Immunol. 2008; 59:90-8.
51. Saito S, Shima T, Nakashima A, et al. What is the role of regulatory T cells in the success of implantation and early pregnancy?. J Assist Reprod Genet. 2007; 24:379-86.
52. LinksKämmerer U. Antigen-presenting cells in the decidua. Chem Immunol Allergy. 2005; 89:96-104.
53. Ha CT, Waterhouse R, Wessells J, et al. Binding of pregnancy-specific glycoprotein 17 to CD9 on macrophages induces secretion of IL-10, IL-6, PGE2, and TGF-beta1. J Leukoc Biol. 2005; 77:948-57.
54. Sharony R, Zadik I, Parvari R. Congenital deficiency of alpha feto-protein. Eur J Hum Genet. 2004; 12:871- 4.
55. Sarafana S, Coelho R, Neves A, et al. Gestational immunology. Acta Med Port. 2007; 20: 355-8.
56. Linksvon Rango U. Fetal tolerance in human pregnancya crucial balance between acceptance and limitation of trophoblast invasion. Immunol Lett. 2008; 115(1):21-32.
57. Borth W. Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J. 1992; 6:3345-53.
58. Elangovan N, Lee YC, Tzeng WF et al. Delivery of ferric ion to mouse spermatozoa is mediated by lipocalin internalization. Biochem Biophys Res Commun. 2004; 319: 1096-1104.
59. Misra UK, Gonzalez-Gronow M, Gawdi G, et al. A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates alpha2M*-induced signalling. Cell Signal. 2004; 16:929-38.
60. Misra UK, Gonzalez-Gronow M, Gawdi G, et al. The role of MTJ-1 in cell surface translocation of GRP78, a receptor for alpha 2-macroglobulin-dependent signaling. J Immunol. 2005; 174:2092-7.
61. Ryon J, Bendickson L, Nilsen-Hamilton M. High expression in involuting reproductive tissues of uterocalin/24p3, a lipocalin and acute phase protein. Biochem J. 2002; 367(Pt 1):271-7.
62. Lee YC, Liao C Jr, Li PT, et al. Mouse lipocalin as an enhancer of spermatozoa motility. Mol Biol Rep. 2003; 30:165-72.
63. Lee YC, Elangovan N, Tzeng WF et al. Mouse uterine 24p3 protein as a suppressor of sperm acrosome reaction. Mol Biol Rep. 2005; 32: 237-45.
64. Fouchécourt S, Charpigny G, Reinaud P, et al. Mammalian lipocalin-type prostaglandin D2 synthase in the fluids of the male genital tract: putative biochemical and physiological functions. Biol Reprod. 2002; 66: 458-67.
65. Sundaram M, van Aalten DM, Findlay JB et al. The transfer of transthyretin and receptor-binding properties from the plasma retinol-binding protein to the epididymal retinoic acid-binding protein. Biochem J. 2002; 362: 265-71.
66. Suzuki K, Lareyre JJ, Sanchez D et al. Molecular evolution of epididymal lipocalin genes localized on mouse chromosome 2. Gene. 2004; 339:49-59.
67. Yu X, Gupta A, Wang Y, et al. Foxa1 and Foxa2 interact with the androgen receptor to regulate prostate and epididymal genes differentially. Ann N Y Acad Sci. 2005; 1061:77-93.
68. Suzuki K, Yu X, Chaurand P et al. Epididymis-specific promoter-driven gene targeting: A transcription factor which regulates epididymis-specific gene expression. Mol Cell Endocrinol 2006;250:184-9.
69. Suzuki K, Yu X, Chaurand P, Araki Y, et al. Epididymisspecific lipocalin promoters. Asian J Androl. 2007; 9:515-21.
70. Drevon CA. Fatty acids and expression of adipokines. Biochim Biophys Acta. 2005; 1740: 287-92.
71. Cho YM, Youn BS, Lee H, et al. Plasma retinol-binding protein-4 concentrations are elevated in human subjects with impaired glucose tolerance and type 2 diabetes. Diabetes Care. 2006; 29:2457-61.
72. Krzyzanowska K, Zemany L, Krugluger W, et al. Serum concentrations of retinol-binding protein 4 in women with and without gestational diabetes. Diabetologia. 2008; 51:1115-22.
73. Ueland T, Dalsoren T, Voldner N, et al. Retinol-binding protein-4 is not strongly associated with insulin sensitivity in normal pregnancies. Eur J Endocrinol. 2008; 159:49-54.
74. García GA, Gaitán A. Biología feromonal en la especie humana. Repert med cir. 2008; 17: 72-89.
75. McClintock MK. Menstrual synchrony and suppression. Nature. 1971; 229: 244-45.
76. McClintock MK. Estrous synchrony and its mediation by airborn chemical communication (Rattus norvegicus). Horm Behav.1978; 10: 264-76.
77. Graham CA, McGrew WC. Menstrual synchrony in female undergraduates living on a coeducational campus. Psychoneuroendocrinology. 1980; 5: 245-52.
78. Schmale H, Ahlers C, Blaker M et al. Perireceptor events in taste. Ciba Found Symp. 1993; 179:167-80.
79. Quadagno DM, Shubeita HE, Deck J, et al. Influence of male social contacts, exercise and all-female living conditions on the menstrual cycle. Psychoneuroendocrinology. 1981; 6: 239-44.
80. Zeng C, Spielman AI, Vowels BR, et al. A human axillary odorant is carried by apolipoprotein D. Proc Nat Acad Sci USA. 1996; 93: 6626-30.
81. Briand L, Eloit C, Nespoulous C, et al. Evidence of an odorant-binding protein in the human olfactory mucus: location, structural characterization, and odorantbinding properties. Biochemistry. 2000; 41: 7241-52.
82. Brennan PA. The vomeronasal system. Cell Mol Life Sci. 2001; 58: 546-55.
83. Duque Parra JE, Duque Parra CA. Nervio terminal: el par craneal cero. MedUNAB. 2006; 3: 246-9.
84. Mundy NI. Genetic basis of olfactory communication in primates. Am J Primatol. 2006; 68:559-67.
85. Cavaggioni A, Mucignat C, Tirindelli R. Pheromone signalling in the mouse: role of urinary proteins and vomeronasal organ. Arch Ital Biol. 1999;137:193-200.
86. Cavaggioni A, Mucignat-Caretta C. Major urinary proteins, alpha(2U)-globulins and aphrodisin. Biochim Biophys Acta. 2000;1482: 218-28.
87. Beynon RJ, Hurst JL. Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans. 2003; 31:142-6.
88. Beynon RJ, Hurst JL. Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 2004; 25:1553-63.
89. Briand L, Trotier D, Pernollet JC. Aphrodisin, an aphrodisiac lipocalin secreted in hamster vaginal secretions. Peptides. 2004; 25:1545-52.
90. Armstrong SD, Robertson DH, Cheetham SA, et al. Structural and functional differences in isoforms of mouse major urinary proteins: a male-specific protein that preferentially binds a male pheromone. Biochem J. 2005; 391(Pt 2):343-50.
91. Kristensen K, Wide-Swensson D, Schmidt C, et al. Cystatin C, beta-2-microglobulin and beta-trace protein in pre-eclampsia. Acta Obstet Gynecol Scand. 2007; 86: 921-6.
92. Chen DY, Wang JJ, Huang YF, et al. Relationship between lipocalin-type prostaglandin D synthase and alpha-glucosidase in azoospermia seminal plasma. Clin Chim Acta. 2005; 354:69-76.
93. Heshmat SM, Mullen JB, Jarvi KA et al. Seminal plasma lipocalin-type prostaglandin D synthase: a potential new marker for the diagnosis of obstructive azoospermia. J Urol. 2008; 179:1077-80.
94. Kim J, Yang P, Suraokar M, et al. Suppression of prostate tumor cell growth by stromal cell prostaglandin D synthase-derived products. Cancer Res. 2005; 65:6189-98.
95. Suzuki T, Hayashi S, Miki Y, et al. Peroxisome proliferator-activated receptor gamma in human breast carcinoma: a modulator of estrogenic actions. Endocr Relat Cancer. 2006; 13:233-50.
96. Shiki Y, Shimoya K, Tokugawa Y, et al. Changes of lipocalin-type prostaglandin D synthase level during pregnancy. J Obstet Gynaecol Res. 2004; 30: 65-70.